Import risk assessment: Unrestric ted imports ofruminan, swine, and poultry meat and meat products fr om the Eur opean Union This page is intentionally blank Primary author:

Stephen Cobb BSc(VetSci) BVM&S MRCVS, Director, SRC Associates

Prepared for:

A t v in n u v e g a - og NÝSKÖPUNARRÁÐUNEYTIÐ Ministry of Industries and Innovation This page is intentionally blank CONTENTS

1. Executive summary

2. Introduction 3. Scope 4. Commodity definition 5. Methodology 6. Preliminary hazard list

7. African swine fever virus 8. Aujeszky’s disease virus 9. Avian encephalomyelitis virus 10. Avian infectious bronchitis virus 11. Avian influenza virus 12. Avian m etapneum ovirus 13. Avian paramyxoviruses (except Newcastle disease virus) 14. Border disease virus 15. Bovine viral diarrhoea virus 16. Capripoxvirus 17. Classical swine fever virus 18. Crimean Congo haemorrhagic fever virus 19. Duck adenovirus A (egg drop syndrome) 20. Duck hepatitis virus 21. D uck virus enteritis virus 22. Foot and mouth disease virus 23. Infectious bursal disease virus 24. Newcastle disease virus 25. Nipah virus 26. Peste des petits ruminants virus 27. Porcine epidemic diarrhoea virus 28. Porcine reproductive and respiratory syndrome virus 29. Porcine teschovirus 30. Swine vesicular disease virus 31. Transmissible gastroenteritis virus 32. Vesicular exanthema of swine virus 33. Vesicular stomatitis virus

34. B a cill us anthracis 35. B r u c e ll a spp.

1 36. C h la m y d o p h i la a b o r tu s 37. C ox iell a b u r n e ti i 38. L e p to sp ir a spp. 39. M ycobacterium bovis 40. M y co p la s m a spp. (O IE-Listed) 41. M y co p la s m a spp. (Non OIE-Listed avian isolates) 42. Pasteurelia m ultocida 43. Salmonella abortus ovis 44. S a lm o n ella G allinarum -Pullorum

45. The agent of bovine spongiform encephalopathy 46. E ch i nococcus granulosus 47. Neospora can in u m 48. T a en ia spp. (T. ovis, T. sag i n a ta , and T s o li um ) 49. Trich i n e lla spp.

50. APPENDIX 1 - ICELANDIC REGULATION NO. 448/2012 51. APPEND IX 2 - CH A PTE R 2.1 OF T H E OIE TERRESTRIAL ANIMAL HEALTH CODE

11 1. EXECUTIVE SUMMARY

Currently, imports of fresh meat into Iceland are not Viruses permitted although considerable amounts of meat are • African swine fever virus imported1 that has been subject to freezing for a 30 • Aujeszky’s disease virus day period. The European Free Trade Association • Avian encephalomyelitis virus Surveillance Authority (ESA) has challenged the • Avian infectious bronchitis virus scientific justification for Iceland’s current import policy for raw meat and other raw animal products as • Avian influenza virus set out in Icelandic Regulation No. 448/2012 (on • Avian metapneumovirus measures to prevent the introduction of animal • Avian paramyxoviruses (except Newcastle diseases and contaminated products to Iceland)2. As disease virus) a signatory to the World Trade Organization’s • Border disease virus Agreement on the Application of Sanitary and • Bovine viral diarrhoea virus Phytosanitary Measures (the “SPS Agreement”), • Capripoxvirus Iceland must base its SPS measures on an appropriate • Classical swine fever virus assessment of the actual risks involved, and, if • Crimean Congo haemorrhagic fever virus requested, make known what factors have been taken into consideration, the assessment procedures used, • Duck adenovirus A (Egg drop syndrome) and the level of risk determined to be acceptable. • Duck hepatitis virus • Duck virus enteritis virus This document examines the biological risks • Foot and mouth disease virus associated with the unrestricted3 import of ruminant, • Infectious bursal disease virus swine, and poultry meat from the European Union. • Newcastle disease virus Detailed discussion of risk management measures to • Nipah virus provide the appropriate level of protection against • Peste des petits ruminants virus these identified risks is outside the scope of this assessment. The methodology followed in this • Porcine epidemic diarrhoea virus document follows the guidelines described in Chapter • Porcine reproductive and respiratory 2.1 of the World Organisation for Animal Health syndrome virus (OIE) Terrestrial Animal Health Code4. • Porcine teschovirus • Swine vesicular disease virus This assessment begins with the construction of a • Transmissible gastroenteritis virus preliminary hazard list that includes the 69 OIE- • Vesicular exanthema of swine virus Listed diseases that are associated with ruminants, • Vesicular stomatitis virus swine, and poultry together with 60 other diseases that are considered to be of concern to Iceland, Bacteria namely those diseases listed under Iceland’s domestic legislation (Act No. 25/1993). After consideration of • Bacillus anthracis this preliminary hazard list, the following organisms • Brucella spp. were identified as requiring further analysis to • Chlamydophila abortus determine if they should be identified as potential • Coxiella burnetii hazards: • Leptospira spp. • Mycobacterium bonis • Mycoplasma spp. (OIE-Listed) • Mycoplasma spp. (Non OIE-Listed avian

1 For example, between 1 November 2011 and 28 February 2012, isolates) Iceland imported 150 tonnes of pig meat, 138 tonnes of chicken • Pasteurella multocida (Haemorrhagic meat, 38 tonnes of turkey meat, and 20 tonnes of beef from the septicaemia) European Union. • Salmonella abortus oris 2 Icelandic Regulation No. 448/2012 is reproduced in full in • Salmonella Gallinarum-Pullorum Appendix 1 of this document.

3 This risk assessment assesses the biosecurity risks associated with Other chilled or frozen meat and meat products derived from ruminants, • The agent of bovine spongiform swine, or poultry that have passed ante-mortem and post-mortem encephalopathy inspection in slaughter and processing plants approved for export, which operate effective Good Manufacturing Practice (GMP) and • Neospora caninum Hazard Analysis and Critical Control Point (HACCP) programmes. • E chinococcus granulosus There is no examination of the effectiveness of any internal EU • Taenia spp. (T. oris, T. saginata, and T. solium) legislation that may offer some protection against the identified risks. • Trichinella spp.

4 Chapter 2.1 of the current OIE Terrestrial Animal Health Code is included as Appendix 2 of this document.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union After consideration of the epidemiology of these As a result of individual risk assessments for each agpnts, the following pathogens were identified as potential hazard, the following pathogens have been potential hazards in unrestricted imports of ruminant, assessed to be risks if unrestricted imports of swine, and poultry meat from the European Union ruminant, swine, and poultry meat from the and were subject to individual risk assessments: European Union were permitted:

Viruses • African swine fever virus (imports of pig • African swine fever virus meat) • Avian infectious bronchitis virus • Brucella spp. (imports of ruminant or pig • Avian influenza virus meat) • Avian paramyxoviruses 2, 3, 4, 6, and 7 • Classical swine fever virus (imports of pig • Bovine viral diarrhoea virus meat) • Classical swine fever virus • Highly pathogenic avian influenza virus • Duck hepatitis virus (imports of poultry meat) • Duck virus enteritis virus • Newcastle disease virus (imports of poultry meat) • Infectious bursal disease virus • Porcine reproductive and respiratory • Newcastle disease virus syndrome virus (imports of pig meat) • Porcine reproductive and respiratory • Swine vesicular disease virus (imports of pig syndrome virus meat) • Swine vesicular disease virus • Taenia oils (imports of sheep or goat meat) Bacteria • Trichinella spp. (imports of pig meat) • Bacillus anthrads As noted above, consideration of appropriate • Brucella spp. measures to manage these risks is beyond the scope • Mycoplasma gallisepticnm of this document. Furthermore, there are a number • Mycoplasma anatis of European Union Council Directives that govern • Mycoplasma iotvae measures to be taken within the European Union in • Mycoplasma mekagridis the face of a disease outbreak to minimise the • Salmonella Gallinarum-Pullorum likelihood of disease dissemination through international trade. These measures are likely to have Other a significant impact on the likelihood of introducing a • The agent of bovine spongiform number of the diseases identified above. However, encephalopathy an assessment of whether these measures alone are sufficient to meet Iceland’s appropriate level of • Neospora caniniim protection is beyond the scope of this report and is • Echinococcus granulosus rightly a decision for the Competent Authority in • Taenia spp. (T. avis, T. saginata, and T. solium) Iceland. • Trichinella spp.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 2. INTRODUCTION

The native livestock breeds of Iceland, well known they took into consideration, the assessment for their great genetic diversity and adaptability to procedures they used, and the level of risk they Nordic conditions, have historically played an determined to be acceptable. Although many important role in the food security of the country. governments already use risk assessment in their This particularly applies to the Icelandic sheep and management of food safety and animal and plant Icelandic dairy cattle while the Icelandic horse has health, the SPS Agreement encourages the wider use gained an international reputation in sport and of systematic risk assessment among all WTO tourism. These unique breeds, together with member governments and for all relevant products. endangered goat and poultry populations of heritage value, are free from several diseases and they are MAST has recognised a need to develop import risk likely to be susceptible to foreign pathogens due to assessments to examine the actual risks associated their isolation. Their conservation is strongly with a range of imported commodities including raw supported by utilization in Icelandic agriculture and meat and products containing or consisting of raw any threats such as due to the importation of raw meat from cattle, sheep, pigs, horses, poultry and wild meat and live animals are viewed with concern. animals, unpasteurized eggs and products made from Reflecting this, the importation of animals and animal unpasteurized eggs, which have not been heat treated products into Iceland is strictly controlled. or received equivalent treatment, and unpasteurized milk and products made from unpasteurized milk, The European Free Trade Association Surveillance which have not been heat treated or received Authority (ESA) has challenged the scientific equivalent treatment. justification for Iceland’s current stringent import policy for raw meat and other raw animal products as This qualitative import risk assessment is limited to a set out in Icelandic Regulation No. 448/2012 (on consideration of the risks associated with the measures to prevent the introduction of animal importation of ruminant, swine, and poultry meat and diseases and contaminated products to Iceland). meat products from European Union member countries5. It is anticipated that subsequent import Article 9 of Icelandic Regulation No. 448/2012 risk assessments may be developed to examine the requires that the recommendations of the Icelandic biosecurity risks associated with the other Food and Veterinary Authority (MAST) concerning commodities described above. disease control must be based on risk assessment which, among other things, takes account of lists of the World Organisation for Animal Health (OIE) of A and B diseases and other international standards and guidelines. The implementation of this Article shall be consistent with the provisions of the Agreement on the Application of Sanitary and Phytosanitary Measures (the “SPS Agreement”) in Annex 1A of the Agreement Establishing the World Trade Organization.

The SPS Agreement allows countries to set their own standards. But it also says regulations must be based on science. They should be applied only to the extent necessary to protect human, animal or plant life or health. And they should not arbitrarily or unjustifiably discriminate between countries where identical or similar conditions prevail. Member countries are encouraged to use international standards, guidelines, and recommendations where they exist. However, members may use measures which result in higher standards if there is scientific justification. They can also set higher standards based on appropriate assessment of risks so long as the approach is consistent, not arbitrary. 5 At the time of writing, the 28 member states of the European Countries must establish SPS measures on the basis Union are Austria, Belgium, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, Estonia, Finland, France, Germany, Greece, of an appropriate assessment of the actual risks Hungary, Ireland, Italy, Latvia, Lithuania, Luxembourg, Malta, involved, and, if requested, make known what factors Netherlands, Poland, Portugal, Romania, Slovakia, Slovenia, Spain, Sweden, and United Kingdom.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 3. SCOPE

The scope of this qualitative risk assessment is the Detailed discussion of risk management measures to assessment of the likelihood and consequences of provide the appropriate level of protection against organisms that may be associated with the identified risks is outside the scope of this importation of ruminant, swine, or poultry meat and assessment. meat products being introduced into Iceland as a result of these imports. The risk assessment is undertaken in accordance with the principles and obligations under the World Trade Organisation Agreement on the Application of Sanitary and Phytosanitary Measures.

4. COMMODITY DEFINITION

This document assesses the biosecurity risks Ruminants are restricted to sheep, goats, cattle, associated with chilled or frozen meat6 and meat buffaloes, and deer. The definition of swine includes products7derived from ruminants, swine, or poultry all Sus scrofa. Poultry are defined here as chickens that have passed ante-mortem and post-mortem (Gallusgallus), turkeys (Meleagrisgallopavo gallopava), or inspection in slaughter and processing plants ducks (Pekin ducks, Anas platyrhynchos domestica or approved for export, which operate effective Good Anas peking, Muscovy ducks Cairina moschata, or a Manufacturing Practice (GMP) and Hazard Analysis hybrid of these known as mulard or moulard ducks). and Critical Control Point (HACCP) programmes8.

6 Skeletal muscle with naturally included or inherent tissue or bone. This definition excludes animal by-products, offal, and giblets.

7 Products prepared from or with meat that has undergone treatment such that the cut surface shows that the product no longer has the characteristics of fresh meat (e.g. cooked or cured).

8 For example, based on Codex Alimentarius guidelines for the control of Campylobacter and Salmonella in chicken meat, CAC/GL 78-2011.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 5. METHODOLOGY

The methodology followed in this document follows As described by the OIE, risk analysis is considered the guidelines described in Chapter 2.1 of the World to consist of four components, namely hazard Organisation for Animal Health (OIE) Terrestrial identification, risk assessment, risk management, and Animal Health Code (OIE 2012a) and further risk communication (Figure 1). As discussed above, discussed in Import Risk Analysis: Animals and Animal risk management is outside the scope of this work, Products (Murray 2002) and the OIE Handbook on which is constrained to the first two of these stages, Import Risk Analysis fo r Animals and Animal Products hazard identification and risk assessment. (OIE 2004). Figure 1. The four components of risk analysis (OIE 2012a)

) I I

Risk communication

5.1. PRELIMINARY HAZARD LIST

This process begins with the construction of a preliminary hazard list derived from the OIE-Listed c. The disease has been shown to, or diseases that are associated with ruminants, swine, scientific evidence indicates that it and poultry (Table 1). The objective of listing would, cause significant morbidity or diseases is to support OIE member’s efforts to mortality in wild animal populations; prevent the spread of important transboundary AND animal diseases. Article 1.2.2 of the OIE Code (OIE 2012b) explains that the criteria for listing a disease 4. A reliable means of detection and are. diagnosis exists and a precise case definition is available to clearly identify 1. International spread of the agent (via cases and allow them to be live animals or their products, vectors distinguished from other diseases, or fomites) has been proven; AND infections and infestations; OR

2. At least one country has demonstrated 5. The disease or infection is an emerging freedom or impending freedom from disease with evidence of zoonotic the disease, infection or infestation in properties, rapid spread, or significant populations of susceptible animals, morbidity or mortality and a case based on the animal health surveillance definition is available to clearly identify provisions of the Terrestrial Code, in cases and allow them to be particular those contained in Chapter distinguished from other diseases or 1.4; AND EITHER infections.

3. a. Natural transmission to humans has In addition to the OIE-listed diseases, the preliminary been proven, and human infection is hazard list in this assessment also includes a list of associated with severe consequences; other diseases that are considered to be diseases of OR concern to Iceland, namely those diseases listed under Iceland’s domestic legislation (Act No. b. The disease has been shown to cause 25/1993) (Table 2). significant morbidity or mortality in domestic animals at the level of a The diseases/agents of interest are those that are country or a zone; OR thought to be exotic to Iceland and, based on their

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union likely ability to be transmitted by direct contact, 4. Consistency in risk assessment indirect contact, or ingestion, could be transmitted in methods should be encouraged and meat or meat products and could infect domestic, transparency is essential in order to feral, or wild animals that occur in Iceland, or ensure fairness and rationality, humans. consistency in decision making and ease of understanding by all the Organisms in the preliminary hazard list requiring interested parties. further consideration are subjected to further analysis 5. Risk assessments should document the to determine whether they should be identified as uncertainties, the assumptions made, potential hazards and all organisms identified as and the effect of these on the final risk potential hazards are subjected to risk assessment. estimate. 6. Risk increases with increasing volume of commodity imported. 5.2. HAZARD IDENTIFICATION 7. The risk assessment should be amenable to updating when additional The process of hazard identification results in the information becomes available. identification of pathogenic agents which could potentially cause adverse consequences associated In line with the OIE risk analysis methodology, for with the importation of the commodity defined in each potential hazard requiring risk assessment the Section 4 of this document. following analysis is carried out:

For each organism from the preliminary hazard list a) Entry assessment - the likelihood of identified as requiring further consideration in Table the organism being imported in the 1 and Table 2, the epidemiology is discussed to commodity. determine which of these organisms should be b) Exposure assessment - the likelihood identified as a potential hazard in imported meat and of animals or humans in Iceland being meat products. exposed to the organism. c) Consequence assessment - the Hazard identification is a categorisation step, consequences of entry, establishment identifying biological agents dichotomously as or spread of the organism9. potential hazards or not. Any agents identified as a d) Risk estimation - a conclusion on the potential hazard are then subject to risk assessment. risk posed by the organism based on the release, exposure and consequence 5.3. RISK ASSESSMENT assessments. If the risk estimate is non-negligible, then the organism is classified as a risk. Article 2.1.3 of the OIE Code (OIE 2012a) identifies the following principles of risk assessment: It is important to note that all of the above steps may not be necessary in all risk assessments. The OIE 1. Risk assessment should be flexible to risk analysis methodology makes it clear that if the deal with the complexity of real life likelihood of entry is negligible for a potential hazard, situations. No single method is then the risk estimate is automatically negligible and applicable in all cases. Risk assessment the remaining steps of the risk assessment need not should be able to accommodate the be carried out. The same situation arises where the variety of animal commodities, the likelihood of entry is non-negligible but the exposure multiple hazards that may be identified assessment concludes that the likelihood of exposure with an importation and the specificity to susceptible species in the importing country is of each disease, detection and negligible, or where both entry and exposure are non- surveillance systems, exposure negligible but the consequences of introduction are scenarios and types and amounts of concluded to be negligible. data and information. 2. Both qualitative risk assessment and quantitative risk assessment methods 5.3.1. Entry assessment are valid. 3. The risk assessment should be based The entry assessment describes the biological on the best available information that pathway(s) necessary for an importation activity to is in accord with current scientific introduce pathogenic agents into a particular thinking. The assessment should be well-documented and supported with references to the scientific literature 9 Detailed analysis of the estimated consequences is not necessary and other sources, including expert if there is sufficient evidence, or it is widely agreed, that the opinion. introduction of a hazard will have unacceptable consequences. In such cases, risk assessment will primarily focus on the likelihood of entry, establishment and exposure.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union environment, and estimates the likelihood of that c. Commodity factors complete process occurring. Examples of the factors ■ quantity of commodity to be that may be considered in the entry assessment are. imported ■ intended use of the imported a. Biological factors animals or products ■ species, age and breed of animals ■ disposal practices. ■ agent predilection sites ■ vaccination, testing, treatment and If the exposure assessment demonstrates no quarantine. significant risk, the risk assessment may conclude at b. Country factors this step. ■ incidence or prevalence ■ evaluation of Veterinary Services, 5.3.3. Consequence assessment surveillance and control programmes and zoning and compartmentalisation systems of The consequence assessment describes the the exporting country. relationship between specified exposures to a c. Commodity factors biological agent and the consequences of those exposures. A causal process should exist by which ■ quantity of commodity to be exposures produce adverse health or environmental imported consequences, which may in turn lead to socio­ ■ ease of contamination economic consequences. The consequence ■ effect of processing assessment describes the potential consequences of a ■ effect of storage and transport. given exposure and estimates the likelihood of them occurring. Examples of consequences include: If the entry assessment demonstrates no significant risk, the risk assessment does not need to continue. a. Direct consequences ■ animal infection, disease and 5.3.2. Exposure assessment production losses ■ public health consequences. The exposure assessment describes the biological b. Indirect consequences pathway(s) necessary for exposure of animals and ■ surveillance and control costs humans in Iceland to the pathogenic agents from ■ compensation costs imported meat and meat products, and estimates the ■ potential trade losses likelihood of the exposure(s) occurring. Examples of ■ adverse consequences to the the factors that may be considered in the exposure environment. assessment are. 5.3.4. Risk estimation a. Biological factors ■ properties of the agent. The risk estimation integrates the results from the b. Country factors entry assessment, exposure assessment, and ■ presence of potential vectors consequence assessment to produce an overall ■ human and animal demographics measure of risk associated with the hazard identified ■ customs and cultural practices at the outset. Thus risk estimation takes into account ■ geographical and environmental the whole of the risk pathway from hazard identified characteristics. to unwanted outcome.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 6. PRELIMINARY HAZARD LIST

As discussed above, the first step in this assessment is the current OIE-listed diseases (Table 1) and a list of hazard identification. This process begins with the animal diseases identified by Icelandic experts as collation of a list of organisms that might be being of significant concern (Table 2). associated with ruminant, swine, or poultry meat (the preliminary hazard list). The diseases/agents of Organisms in the preliminary hazard list requiring interest are those that could be transmitted in meat or further consideration are subjected to further analysis meat products and could infect domestic, feral, or to determine whether they should be identified as wild animals that occur in Iceland, or humans. In this potential hazards and all organisms identified as case the preliminary hazard list was compiled from potential hazards are subjected to risk assessment.

Table 1. OIE-Listed diseases associated with ruminants, swine, and poultry (OIE 2012b)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

African swine fever Domestic pigs, Never Direct and indirect Yes Penrith et al. 2004; African swine fever virus European wild reported contact, vectors Sánchez -Vizc aíno (ASFV) (only member of the boars, and feral (Ornithodoros spp.), 2006; Kleiboeker Asfarviridae family, genus pigs and ingestion 2008; Oura and Asfivirus) Arias 2012

Anthrax Mainly herbivores, Last Ingestion or Yes De Vos and Bacillus anthracis although can affect reported inhalation Turnbull 2004; all mammals, and 2004 Golsteyn-Thomas some avian species and Harvey 2012

Aujeszky’s disease Primarily pigs (but Never Direct and indirect Yes Donaldson et al. Suid herpesvirus 1 (Aujeszky’s may infect a reported contact, possibly 1983; Davison et al. disease virus, ADV) variety of ingestion. 2005; Jestin and Le mammals (such as Potier 2012 dogs, cats, cattle, sheep, rabbits, foxes, minks, etc.)

Avian chlamydiosis Primarily avian Never Inhalation No Andersen and Chlamydophila psittaci species reported Vanrompay 2008; Cobb 2011; Sachse 2012

Avian infectious Chickens Last Air-borne, direct and Yes Cavanagh 2005; bronchitis reported indirect contact Gelb 2008; Cobb Avian infectious bronchitis virus 1998 2011 (IBV) Avian infectious Principally Never Principally No Jones 2008; Cobb laryngotracheitis chickens, also reported respiratory 2011; King et al. Gallid herpesvirus 1 (Infectious pheasants, 2012a laryngotracheitis virus, ILTV) partridges, and peafowl

Avian influenza All avian species, Never Direct or indirect Yes Easterday et al. 1997; Avian influença (AI) virus most frequently reported contact, aerosols, Fauquet et al. 2005b; (members of the family waterfowl and ingestion Swayne and Beck Orthomyxoviridae; in the genus 2005 ; Cobb 2011; Influenzavirus A) Swayne 2012

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Avian mycoplasmosis Gallinaceous birds, Last Vertically through Yes Levisohn and Mycoplasma gallisepticum especially reported infected eggs; Kleven 2000; Kleven commercial 1994 horizontally by close and Bradbury 2008; chickens and contact Cobb 2011 turkeys, also pheasants, peafowl, quail, ducks, geese

Avian mycoplasmosis Principally Never Vertically through Yes Bradbury and Mycoplasma synoviae chickens and reported infected eggs; Morrow 2008; turkeys horizontally by close Kleven and contact Bradbury 2008; Cobb 2011

Bluetongue Domestic and wild Never Vector (midges of No Daniels and Oura Bluetongue virus (BTV) ruminants such as reported certain species in the 2009 (member of the Orbivirus sheep, goats, cattle, genus Culicoides) genus of the family buffaloes, deer, Reoviridae). The BTV species, most species of or serogroup, contains 24 African antelope recognised serotypes and various other Artiodactyla as vertebrate hosts

Bovine anaplasmosis Cattle Never Mechanical or No McElwain 2012 Mainly Anaplasma marginale. reported biological by Also Anaplasma centrale and arthropod vectors Anaplasma phagocytophilium (ticks) (Family Anaplasmataceae; Order Rickettsiales)

Bovine babesiosis Cattle Never Vectors (Rhipicephalus No De Vos et al. 2004; Babesia bovis, reported spp., Ixodes ricinus, Rolls et al. 2010 B. bigemina, B. divergens and Haemaphysalis spp.) others

Bovine genital Cattle Never Venereal No Irons et al. 2004; campylobacteriosis reported transmission Wagenaar and Van Campylobacterfetus subsp. Bergen 2008 venerealis

Bovine spongiform Cattle Never Oral Yes Bradley and encephalopathy reported Verwoerd 2004; The disease agent causing Simmons et al. 2010; bovine spongiform Wilesmith et al. 2010 encephalopathy (BSE) is generally accepted to be a prion

Bovine tuberculosis Cattle, other Last Aerosol exposure Yes Cousins 2009 Mycobacterium bovis domesticated reported and ingestion animals 1959 and certain free or captive wildlife species

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Bovine viral diarrhoea Cattle. Pigs,deer, Never Direct contact and Yes Horner 2000; Le Bovine viral diarrhoea virus sheep, and goats reported possibly by ingestion Potier et al. 2006; (BVDV) (a Pestivirus in the also susceptible Radostits et al. 2007a; family Flaviviridaê) Drew 2008b; Bratcher et al. 2012; Simmonds et al. 2012

Brucellosis (bovine) Catle. Also camels, Never Oral, respiratory, or Yes Nielsen and Ewalt Brucella abortus, less llama, alpaca, reported conjunctival 2009 frequently by B. melitensis, guanaco, and transmission and occasionally by B. suis vicuna as well as domestic buffalo, American and European bison, yak, elk/wapiti, African buffalo, and various African antelope species

Brucellosis (ovine and Sheep and goats Never Oral, respiratory, or Yes Garin-Bastuji and caprine) reported conjunctival Blasco 2009a Brucella melitensis (biovars 1, 2 transmission or 3), also (sporadically) B. abortus

Brucellosis (porcine) Pigs Never Mainly oral Yes MacMillan et al. Brucella suis (five biovars, but reported 2006; Olsen 2009 the infection in pigs is caused by B. suis biovars 1, 2 or 3), rarely also B. melitensis or B. abortus

Caprine Goats Never Principally via No Werling and arthritis/encephalitis reported colostrum or milk Langhans 2004; Caprine arthritis/encephalitis Knowles and virus (CAEV) (Lentivirus) Herrmann 2008a

Classical swine fever Pigs Last Oral and oral-nasal Yes Watt and Wallace Classical swine fever virus reported transmission, direct 1954; Van Oirschot (CSFV) (a member of the 1953 and indirect contact, 2004 genus Pestivirus of the family ingestion Thiel et al. 2005b; Flaviviridae) Drew 2008b

Contagious agalactia Sheep and goats Never Direct contact Yes Timoney et al. 1988b; Mycoplasma agalactiae, also M. reported Nicolas and Loria capricolum subsp. capricolum 2013 (Mcc), M. mycoides subsp. capri (Mmc) (formerly named M. mycoides subsp. mycoides LC) and M. putrefaciens

Contagious bovine Mainly cattle and Never Direct contact Yes Thiaucourt 2008a pleuropneumonia zebu, also reported Mycoplasma mycoides subsp. buffaloes sheep mycoides SC (Mmm SC) and goats, and other wild ruminants

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Contagious caprine Goats Never Direct contact, Yes Thiaucourt 2008b pleuropneumonia reported aerosols Mycoplasma capricolum subspecies capripneumoniae (Mccp)

Crimean Congo Wide variety of Never Vectors (Hyalomma Yes Swanepoel et al. haemorrhagic fever ruminants and reported spp.), also contact 1985; Swanepoel et Crimean Congo haemorrhagic other smaller with infected blood al. 1987; Swanepoel fever virus (CCHFV) (member animals such as and meat and Burt 2004; of the Nairovirus genus) hares Fauquet et al. 2005b

Duck virus hepatitis Ducks (and Never Aerosol or ingestion Yes Woolcock 2008; Most commonly duck turkeys reported Woolcock 2010; hepatitis virus (DHV) type I (a experimentally) Cobb 2011 member of the Picornaviridae in the genus Avihepatovirus). Three serotypes recognised - duck hepatitis A virus (DHAV) types 1, 2 and 3. DHV type II (duck astrovirus type I (DAstV -I)) has been reported in the United Kingdom only. DHV type III (duck astrovirus type II (DAstV-II)) has been reported only in the United States of America

Echinococcosis / Domestic dog and Last Ingestion Yes Taylor et al. 2007a; Hydatidosis a number of reported Kamiya 2008 E chinococcus granulosus domestic ungulate 1979 species

Enzootic abortion of ewes Sheep and goats Never Direct contact, Yes Aitken 1983; (ovine chlamydiosis) less commonly, reported ingestion Radostits et al. Chlamydophila abortus cattle, pigs, horses 2007b; Sachse and and deer Longbottom 2012

Enzootic bovine leukosis Cattle, water Never Direct transfer of No Werling et al. 2004; Bovine leukaemia virus (BLV), buffaloes, and reported blood Vahlenkamp 2012 (a member of the family capybaras. Retroviridae)

Epizootic haemorrhagic Wild ruminants Never Vector (midges of No Daniels and Oura disease reported certain species in the 2009 Epizootic haemorrhagic disease genus Culicoides) virus (EHDV) (member of the Orbivirus genus in the family Reoviridae)

Equine encephalomyelitis Birds and horses. Never Vector (mosquitoes) No Weaver et al. 2005; (Eastern) Sporadic cases reported Ostlund 2013 Eastern equine encephalomyelitis reported in cows, virus (EEEV) sheep, pigs, deer, and dogs.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Foot and mouth disease Cattle, pigs, sheep, Never Direct contact, Yes Gloster et al. 1982; Foot and mouth disease virus goats and water reported exposure to Paton et al. 2011; (FMDV) (member of the buffalo (Bubalus excretions and Paton et al. 2012 genus Aphthovirus, family bubalis) as well as secretions, or Picornaviridaê). There are species of cloven- ingestion. Aerosols seven serotypes of FMD hoofed Outbreaks have been virus (FMdV), namely O, A, Wildlife attributed to infected C, SAT 1, SAT 2, SAT 3, meat and Asia 1

Fowl typhoid Chickens and Last Direct or indirect Yes Shivaprasad and Salmonella Gallinarum biovar turkeys reported contact, ingestion Barrow 2008; Davies Gallinarum (Salmonella 1953 2012 Gallinarum)

Haemorrhagic Cattle and Never Direct contact Yes Singh 2012 septicaemia buffaloes reported Pasteurella multocida

Heartwater Ruminants Never Vector (Amblyomma No Martinez et al. 2008 Ehrlichia ruminantium reported ticks) (formerly Cowdria ruminantium)

Infectious bovine Mainly cattle. Also Present Direct contact and No Beer 2010 rhinotracheitis/ infectious goats, sheep, water venereal pustular vulvovaginitis buffaloes, camelids transmission Bovine herpesvirus 1 (BoHV-1) (a member of the genus Varicellovirus in the family Herpesviridae)

Infectious bursal disease Principally Last Direct or indirect Yes Lukert 1998; (Gumboro disease) chickens. Also reported contact, ingestion Eterradossi 2008; Infectious bursal disease virus Turkeys, ducks, 1998 Eterradossi and Saif (IBDV) (member of the guinea fowl, and 2008 genus Avibirnavirus of the ostriches family Birnaviridae)

Japanese encephalitis Horses, pigs Never Vector (Culex No Thiel et al. 2005a; Japanese encephalitis virus (JEV) reported Tritaeniorhynchus and Kondo 2008 (member of the genus other culicine Flavivirus in the family mosquitoes) Flaviviridae)

Lumpy skin disease Cattle Never Transmission No Tuppurainen 2010 Various strains of reported predominantly by Capripoxvirus insects, natural contact transmission in the absence of insect vectors inefficient

Maedi-visna Sheep Last Principally via No Verwoerd et al. Maedi-visna virus (MVV) reported colostrum or milk 2004b; Knowles and (Lentivirus) 1965 Herrmann 2008b

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Nairobi sheep disease Sheep and goats Never Vector (ticks) No Gerdes 2008 Nairobi sheep disease virus reported (NSDV) (genus Nairovirus, family Bunyaviridae)

New World screwworm Mammals Never Fly strike of wounds. No Geering et al. 1995; Cochliomyia hominivorax reported Larvae unable to Hall 2008 survive outside host

Newcastle disease Infects over 200 Never Direct or indirect Yes Alexander et al. 1984; Newcastle disease virus (NDV) species of birds, reported contact, aerosols Alexander and Senne (virulent strains of avian but the severity of 2008; Afonso et al. paramyxovirus type 1 disease produced 2012 (APMV-1) of the genus varies with both Avulavirus; family host and strain of Paramyxoviridae) virus

Nipah virus encephalitis Pigs, horses, dogs, Never Direct contact Yes Middleton et al. 2002; Nipah virus (a paramyxovirus and cats reported Tan and Wong 2003; in the subfamily Eaton et al. 2006; Paramyxovirinae; genus Wang et al. 2012 Henipavirus)

Old World screwworm Mammals Never Fly strike of wounds. No Geering et al. 1995; Chrysomya bezziana reported Larvae unable to Hall 2008 survive outside host

Ovine epididymitis Sheep, also cattle, Never Mainly venereal Yes Garin-Bastuji and Brucella ovis goats, and deer reported transmission, also Blasco 2009b oral

Paratuberculosis Principally cattle, Present Ingestion No Gwozdz 2008 Mycobacterium sheep, goats (also avium subsp. paratuberculosis horses, pigs, deer (M. paratuberculosis) and alpaca, and recently in rabbits, stoat, fox, and weasel)

Peste des petits ruminants Sheep, goats, and Never Inhalation, close Yes Rossiter 2004; Lamb Peste des petits ruminants virus occasionally wild reported contact. et al. 2005; Diallo (PPRV) (a Morbillivirus in the small ruminants. 2012 family Paramyxoviridae) Also camels, cattle, and buffaloes

Porcine cysticercosis Pigs Never Ingestion Yes Allan et al. 2005; Cysticercus cellulosae reported Taylor et al. 2007

Porcine reproductive and Pigs Never Direct and indirect Yes Magar and respiratory syndrome reported contact, ingestion Larochelle 2004; Porcine reproductive and Snijder et al. 2005; respiratory syndrome virus Ludemann and (PRRSV) (a member of the Lager 2010 order Nidovirales, family Arteriviridae, genus Arterivirus). Two major antigenic types of the virus exist, the type 1 (European) and the type 2 (American)

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Pullorum disease Chickens and Last Direct or indirect Yes Shivaprasad and Salmonella enterica subspecies turkeys reported contact, ingestion Barrow 2008; Davies enterica serovar Gallinarum 1958 2012 biovar Pullorum (Salmonella Pullorum)

Q fever Mostly cattle, Never Inhalation, and Yes Woldehiwet 2004; Coxiella burnetii (Gram­ sheep, and goats reported direct contact. Rousset et al. 2010 negative obligate (although present Ingestion has been intracellular bacterium) in all animal suggested kingdoms)

Rabies All mammals Never Almost always by No Baer 1990; Rabies virus (member of the reported bite. Fragile virus Swanepoel 2004; genus Lyssavirus in the family never reported in Tordo et al. 2005a; Rhabdoviridae) meat Radostits et al. 2007c; Fooks et al. 2011

Rift Valley fever Domestic Never Vector No Gerdes et al. 2008 Rift Valley fever virus (RVFV), ruminants reported a mosquito-borne Bunyavirus of the genus Phlebovirus

Rinderpest Domestic cattle, Never 2011 international No Taylor and Roeder Rinderpest virus, a member of yaks, wild African reported declaration of global 2012 the Morbillivirus genus within buffaloes (Syncerus freedom from the family Paramyxoviridae caffer), and Asian rinderpest. water buffaloes (Bubalus bubalis). Also sheep, goats, pigs, and wild ungulates

Salmonellosis Sheep Never Usually ingestion Yes Linklater 1983 Salmonella abortus ovis reported

Scrapie Sheep Present Ingestion No Detwiler and Baylis The aetiological agent of 2003; Ryder et al. scrapie is considered to be 2004, Evoniuk et al. an infectious prion PrPSC 2005; Hörnlimann et al. 2007

Sheep pox and goat pox Sheep and goats Never Direct contact and Yes Tuppurainen 2012 Strains of Capripoxvirus reported via insects

Surra Camels, horses, Never Arthropod-borne No Desquesnes 2012 Trypanosoma evansi buffalos, and reported disease; several cattle. Other species of animals, including haematophagous wildlife, are also flies, including susceptible Tabanids and Stomoxes

Swine vesicular disease Pigs Never Direct and indirect Yes Stanway et al. 2005; Swine vesicular disease virus reported contact. Ingestion Torres 2008 (SVDV)

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 1. (continued)

Disease and aetiology Animal species Iceland Transmission Consider References infected status further? (OIE 2013)

Theileriosis Wild and domestic Never Vectors (Ixodid ticks) No Pipano et al. 2008 Six identified Theileria spp. Bovidae reported that infect cattle; the two most pathogenic and economically important are T. parva and T. annulata

Transmissible Pigs Never Direct or indirect Yes Spaan et al. 2005; Saif gastroenteritis Transmissible reported faeco-oral and Sestak 2006 gastroenteritis virus (TGEV) transmission (Family. Coronaviridae, Genus: Coronavirus)

Trichinellosis Pigs, rats, bears, Never Ingestion Yes Gajadhar and Forbes Twelve genotypes of walruses, horses reported 2012 Trichinella recognised (occasionally), and including Trichinella spiralis, many other flesh- T. native, T. britovi, T. eating mammals, pseudospiralis, T. murrelli, T. birds, nelson, T. papuae, and T. and reptiles zimbabwensis

Trypanosomosis (tsetse- Principally cattle, Never Vectors (mainly No Desquesnes 2008 transmitted) but also other reported Glossina (tsetse flies), Trypanosoma congolense, T. mammalian but also by several vivax and, to a lesser extent, species biting flies (tabanids, T. brucei brucei stomoxes, etc.).

Trichomonosis Cattle Never Venereal No Gajadhar and Parker Tritrichomonas foetus, a reported transmission 2012 flagellate protozoan

Tularemia Lagomorphs Never Vectors (ticks and No Mörner 2008 Francisella tularensis (rabbits and hares), reported biting flies), direct or rodents, and indirect contact, beavers inhalation, or ingestion

Turkey rhinotracheitis Primarily turkeys Never Direct contact and Yes Pedersen and Avian metapneumovirus and chickens, also reported airborne Eterradossi 2009 (aMPV) (family pheasants, transmission Paramyxoviridae, genus Muscovy ducks, Metapneumovirus) Peking ducks, and guinea fowl

Vesicular stomatitis Sheep, goats, and Never The mechanism of Yes Tordo et al. 2005b; Vesicular stomatitis Alagoas many other wild reported transmission of the Swenson 2010 virus, Vesicular stomatitis species virus is unclear Indiana virus, Vesicular stomatitis New Jersey virus. Many authors regard the three species of virus as serotypes of the same species

West Nile fever Migratory birds, Never Vectors (infections No Thiel et al. 2005a; West Nile virus (WNV) is a horses reported are dependent on Ostlund 2010 member of the genus mosquito Flavivirus in the family transmission) Flaviviridae

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 2. Other (non OIE-Listed) diseases of ruminants, swine, and poultry considered to be of significant concern to Iceland

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Actinomycosis Mainly cattle, Not recognised Commensal No Smith 2012 Actinomyces spp. also horses, (Group C) organisms that swine, dogs, and causes disease sheep through penetrating wounds

Atrophic rhinitis of swine Pigs Present Respiratory No Neumann et al. Bordetella bronchiseptica and (Group C) transmission 2010a Pasteurella multocida (types A and D)

Avian encephalomyelitis Poultry Not recognised Oral-faecal Yes Shafren and Avian encephalomyelitis virus (Group B) transmission Tannock 1991

Avian leucosis Principally Not recognised Vertical No Payne and Avian leukosis virus, Avian chickens, also (Group C) transmission or Venugopal 2000; myeloblastosis virus and Avian pheasants, horizontal Fadley and Nair myelocytomatosis virus 29 partridges, and transmission by 2008 quail direct contact with an infected bird (fragile retrovirus)

Avian mycoplasmosis All avian species Not recognised As with OIE- Yes Goldberg et al. (except M. gallisepticum (Group C) Listed avian 1995; Nicolet and M syno viae) mycoplasmosis, 1996; Stipkovits Class; Mollicutes. The avian vertical and Kempf 1996; Mollicutes are divided into transmission Bradbury and Mycoplasmatales and through infected Morrow 2008; Acholeplasmatales Kleven 2008 In chickens, Mycoplasma horizontally by gallinaceum, M. gallinarum, M. close contact glycophilum, M. iners, M. iowae, M. imitans, M. lipofaciens, M. pullorum, and U. gallorale have been isolated. Mycoplasma meleagridis, M. iowae, M. imitans, M. gallinarum, M. pullorum, and Ureaplasma spp. have been recovered from turkeys and M. anatis, M. cloacale, M. glycophilum, M. imitans, M. lipofaciens, A. axanthum, and A. laidlawii have been isolated from ducks.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Avian paramyxovirus APMV-1 has Not recognised Direct or Yes Alexander and Avian paramyxoviruses except been recovered (Group B) indirect contact, Senne 2008 Newcastle disease virus from a wide aerosols range of avian Nine serogroups of avian species. paramyxoviruses are Chickens have recognised, APMV-1 to been associated APMV-9. Newcastle disease with APMV-2, (ND) is caused by viruses turkeys with belonging to serogroup APMV-2, 3, 6, APMV-1 and 7, ducks with APMV-4, 6, 8, and 9. APMV- 4, 6, and 8 have been recovered from geese, APMV-7 has been associated with pigeons, doves, and ostriches, and APMV-2, 3, and 5 has been recovered from

psittacine species

Avian tuberculosis Chickens, Present M. avium can also No Fulton and Mycobacterium avium turkeys and a (Group B) be transmitted in Sanchez 2008 number of other carcases of avian species tuberculous fowl

Blackleg Cattle and sheep Not recognised Ubiquitous soil No Rodning et al 2011 Clostridium chauvoei (Group C) organism

Border disease Sheep and goats Not recognised Vertical and oro­ Yes Nettleton and Border disease virus (BDV) and (Group A) nasal Willoughby 2008 Bovine viral diarrhoea virus transmission (BVDV) (Pestiviruses in the family Flaviviridae)

Botulism Cattle, sheep, Present Ubiquitous soil No Center for Food Clostridium botulinum horses, mink, (Group C) organism. Security and Public ferrets, Disease caused Health 2006a waterfowl. Less by toxin rather commonly dogs than and pigs transmission of infectious agent

Bovine cysticercosis Cattle act as the Not recognised C. bovis may be Yes Taylor et al. 2007c; saginata intermediate (Group B) found anywhere Lloyd 2008 hosts for T. in striated saginata, the so- muscles of called beef infected cattle tapeworm of humans who are the definitive host.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Bovine respiratory Mainly cattle, Not recognised Respiratory No Valarcher and syncitial virus also sheep, (Group B) transmission Taylor 2007 pneuomonia goats, bison, Bovine respiratory syncytial virus chamoix and (BRSV) (Family camelids Paramyxoviridae; Genus Pneumovirus)

Broken mouth Sheep Present No evidence of No N/A Agents unknown (Group C) infectious aetiology

Caseous lymphadenitis Goats and sheep Not recognised Principally Yes Paton et al. 1995; Corynebacterium (Group C) through wounds, Malone 2007 pseudotuberculosis but inhalation also possible.

Chicken infectious Chickens, Present Vertical No Schat 2012 anaemia possibly (Group C) transmission. Chicken anaemia virus (CAV) Japanese quail Also faecal-oral (Family Circoviridae; Genus and (possibly) Gyrovirus) respiratory horizontal transmission

Clostridiosis All domestic Present Ubiquitous soil No N/A Clostridium spp. excluding C. species (Group C) organisms chauvoei, C. perfringens type C, and C. botulinum

Coccidiosis All commercial Present Faecal-oral No McDougald and Phylum Apicomplexa; Genus poultry species (Group C) transmission Fitz-Coy 2008 Eimeria. Eimeria acervulina, E. brunetti, E. hagani, E. maxima, E. mitis, E. mivati, E. necatrix, E. praecox, and E. tenella are associated with chickens. Eimeria meleagrimitis, E. adenoeides, E. melegridis, E. dispersa, E. gallopavonis are associated with turkeys Eimeria spp., Wenyonella spp., and Tyzzeria spp. are recognised in ducks

Dermatophilosis Many domestic Present Motile zoospore No Timoney et al. Dermatophilus conoglensis species (Group B) form of agent 1988a released when contaminated skin becomes wet

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Duck virus enteritis Waterfowl, Not recognised Natural infection Yes Wobeser and Duck virus enteritis virus principally (Group A) occurs through Docherty 1987; (Anatid Herpesvirus 1/ Duck ducks, geese, and the oral or Richter and Plague Herpesvirus) swans cloacal route, Horzinek 1993; either by direct Fauquet et al. or indirect 2005a; Gough contact 2008; Sandhu and Metwally 2008

Egg drop syndrome Laying hens, Not recognised Vertical Yes Center for Food Duck adenovirus A ducks, and geese (Group B) transmission. Security and Public Also oral and Health 2006b; (possibly) Adair and Smyth respiratory 2008 horizontal transmission

Endemic pneumonia Pigs Present Airborne No Kobisch and Friis Mycoplasma pneumonia (Group C) transmission 1996

Footrot Sheep, goats, Not recognised Acquired from No Bagley 1998 Fusobacterium necrophorum, cattle (Group B) environment Bacteroides melaninogenicus, and contaminated by Dichelobacter nodosus infected animal

Fowl cholera Domesticated Present Direct contact, No Christensen and Pasteurella multoà da and wild avian (Group B) oral and Bisgaard 2000; species respiratory Kunkle and transmission Wilson 2008

Fowlpox Chickens and Not recognised Direct and No Tripathy 2008 Fowlpox virus (Family turkeys (Group B) indirect Poxviridae; Genus mechanical Avipoxvirus) transmission, also mosquitoes

Intestinal salmonellosis All animal Present Food of animal No Davies 2010 Salmonella spp. excluding S. species (Group B) origin is the gallinarum pullorum major source of human Salmonella infections throughout the world (Davies 2010)

Jaagsiekte/Ovine Sheep and Not recognised Retroviruses are No Verwoerd 1990; pulmonary adenomatosis (rarely) goats (Group A) fragile and Verwoerd et al. Jaagsiekte sheep retrovirus survive for only 2004a a short period outside the host. Transmission is by droplet infection, and outbreaks occur when infected sheep are introduced into clean flocks.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Leptospirosis All domestic Not recognised Transmission Yes Greene et al 2006; Leptospira spp. species, humans, (Group B) can occur orally Radostits et al. Before 1989, the species wildlife or through the 2007c Leptospira interrogans skin contained all pathogenic serovars. Now, over 200 serovars of L. interrogans have been re-classified serologically into at least 23 new serogroups based on antigenic relatedness

Listeriosis Clinical Present Oral No Lopez 2008 Listeria monocytogenes listeriosis seen in (Group C) transmission ruminants but infection reported in a wide variety of mammals, birds, fish, and crustaceans

Liver fluke disease Cattle and sheep Not recognised Transmission No Centers for Fasciola hepatica (Group C) requires Disease Control intermediate and Prevention snail host to 2013 complete life cycle

Malignant catarrhal fever Cattle, sheep and Present Direct contact, No Reid and Van Alcelaphine herpesvirus 1 wildebeest (Group B) most likely Vuuren 2004 (AHV-1) and Ovine herpesvirus respiratory 2 (OHV-2) (Family transmission Herpesviridae; Genus Herpesvirus)

Marek’s disease Chickens most Present Virus replicates No Witter 1997; Alphaherpesvirinae, Genus: important (Group B) in feather follicle Witter et al. 2005; Mardivirus, Marek’s disease natural host. epithelial cells. Schat and virus (MDV). Three Other avian Transmission Venugopal 2008 serotypes described, Gallid species follows exposure herpesvirus 2 (serotype1), refractory to to infectious Gallid herpesvirus 3 (serotype infection dust or dander 2) and Meleagrid herpesvirus 1 (serotype 3)

Mastitis-metritis- Pigs Present Complex of No N/A agalactia syndrome (Group C) infections Multiple pathogens acquired immediately post-partum

Melioidosis Sheep, goats, Not recognised Infection No Groves and Burkholderia pseudomallei and pigs (Group C) acquired through Harrington 1994; (formerly Pseudomonas contact with Inglis et al. 2004 pseudomallei and Malleomyces infected pseudomallei) environment

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Necrotic enteritis pigs Not recognised Ubiquitous No Songer and Uzal Clostridiumperfringens type C (Group C) environmental 2005 organism

Neosporosis Cattle and dogs Not recognised Tissue cysts in Yes Dubey et al 2007 Neospora caninum (Group B) intermediate hosts (cattle) transmitted to definitive host (canine) by ingestion

Oedema disease pigs present Oral No Oanh et al 2012 Escherichia coli (Group C) transmission O138/O139/O140/O141

Orf/Contagious echtyma Goats, sheep present Spread by direct No Leite-Browning O rf virus and wild (Group C) and indirect 2008 ruminants contact from infected animals or by contact with infected tissue or saliva containing the virus

Other pasteurellosis Cattle, sheep and present Respiratory No Mohamed and Pasteurella spp. goats (Group C) transmission Abdelsalam 2008

Ovine cysticercosis Sheep and goats Not recognised Oral Yes Lloyd 2008 Taenia ovis act as the (Group B) transmission intermediate recognised hosts for T. ovis. Dogs and wild canids are the definitive hosts.

Parafilariosis Cattle Not recognised Transmission No Caron et al. 2012 Parafilaria bovicola (Group B) requires intermediate host (Musca autumnalis) to feed on secretions of live infected primary host.

Pasteurellosis Cattle, sheep and present Respiratory No Mohamed and Pasteurella multocida and P. goats (Group C) transmission Abdelsalam 2008 haemolytica

Pleuropneumonia pigs present Respiratory No Marsteller and Actinobacillus pleuropneumoniae (Group B) transmission Fenwick 1997; Gottschalk and Taylor 2006

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Porcine epidemic Pigs ? Transmission via Yes Pensaert and Yeo diarrhoea (Group B) the faecal-oral 2006; De Groot et Family Coronaviridae; Genus route al. 2012 Alphacoronavirus. Porcine epidemic diarrhea virus (Pe d v )

Porcine intestinal Pigs Present Faecal-oral No McOrist and adenomatosis (Group C) transmission Gebhart 2006 Lawsonia intracellularis

Porcine parvovirus Pigs Present Faecal-oral No Burgess 1980 infection (Group C) transmission Porcine parvovirus (Family Parvoviridae; Genus Parvovirus)

Pox disease Pigs Not recognised Entry through No Neumann et al. Porcine pox virus (All the (Group C) skin abrasions or 2010b other Poxviridae of livestock; via vectors lumpy skin disease virus, sheep and goat pox, and fowlpox; have been addressed elsewhere)

Ringworm Cattle (and Not recognised Mainly spread by No Wabacha et al. Trichophy ton verrucosum horses) (Group B) contact between 1998 infected and susceptible animals or via a contaminated environment

Sarcoptic mange Pigs Not recognised Transmission by No Soulsby 1969; Sarcoptes scabei var. suis (Group C) direct contact. Blood and Sarcoptic mange Radostits 1989 mites do not survive for more than a few days away from their host

Sheep biting louse Sheep Present Direct contact No Zumpt 1970 Damalinia ovis (Group B) with fleece or indirect via fomites

Sheep keds Sheep Not recognised Direct contact. No Hendrix 2013 Melophagus ovinus (Group B) Keds that fall off the host survive for <1 week

Sheep mange Sheep Present Direct contact No Schlater and Chorioptes ovis (Group B) Mertins 2013

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 2. (continued)

Disease and aetiology Animal species Iceland status Transmission Consider References infected and further? categorisation under Act No 25/1993

Sheep scab Domesticated Not recognised Direct contact No Center for Food Psoroptes ovis (Family sheep (and (Group B) with fleece or Security and Public Psoroptidae; Order Astigmata) bighorn sheep) indirect via Health 2009 fomites

Swine dysentery Pigs Not recognised Multifactoral No Alvarez-Ordóñez Brachyspira hyodysenteriae (Group C) disease with et al. 2013 transmission of fragile Brachyspira by direct contact with infected animals

Swine erysipelas Pigs. E. Present Infection No Wood and Erysipelothrix rhusiopathiae rhusiopathiae may (Group C) acquired from Henderson 2006; also infect sheep, contaminated Lee 2012 lambs and environment turkeys

Swine influenza Pigs Present Primarily an No Thompson and Family: Orthomyxoviridae'; (Group B) infection of the Easterday 2004; Genus: Influenyaiirus A, respiratory Kawaoka et al. Species: Influenya A virus tissues and 2005; Olsen et al. viraemia is not 2006; Zou 2006 considered to be a feature of the disease

Teschen disease Pigs Not recognised Natural infection Yes Alexander 2004; Family Picornaviridae; Genus (Group A) of pigs by Knowles 2008 Teschovirus; Porcine teschovirus enteroviruses is serotype 1 (PTV-1) by the oral route

T oxoplasmosis All warm­ Present Oral No Birgisdóttir et al. Toxoplasma gondii blooded animals (Group C) transmission 2006; Buxton and Maley 2008

Vesicular exanthema of Pigs Not recognised Transmission of Yes Anon 1988; King swine (Group A) infection et al. 2012b Family: Caliciviridae, Genus: through waste Vesivirus. Vesicular food has been exanthema of swine virus described (VESV) and vesiviruses isolated from marine species are phylogenetically grouped together as “marine vesiviruses”

Viral diarrhoea Cattle Present Oral and maybe No Thomas et al. 2006 Coronaviridae (Group B) respiratory

Vomiting and wasting Pigs Not recognised Transmission No Spaan et al. 2005; disease (Group B) occurs through Pensaert 2006 Family: Coronaviridae, Genus: exposure to Coronavirus, Species: Porcine nasal secretions haemagglutinating from infected encephalomyelitis virus pigs

Impoli Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union From the preliminary hazard list (the diseases listed in • Porcine reproductive and respiratory Tables 1 and 2 above), the following organisms syndrome vims require further consideration and will be examined in • Porcine teschovims subsequent Chapters of this document to identify • Swine vesicular disease vims potential hazards in imported ruminant, swine, or • Transmissible gastroenteritis vims poultry meat. All potential hazards will be subject to a risk assessment. • Vesicular exanthema of swine vims • Vesicular stomatitis vims Viruses Bacteria • African swine fever virus • Badilas anthracis • Aujeszky’s disease virus • Brucella spp. • Avian encephalomyelitis virus • Chlamydophila abortas • Avian infectious bronchitis virus • Coxiella burnetii • Avian influenza virus • Leptospira spp. • Avian metapneumovirus • Mycobacterium bonis • Avian paramyxoviruses (except Newcastle • Mycoplasma spp. (OIE-Listed) disease virus) • Mycoplasma spp. (Non OIE-Listed avian • Border disease virus isolates) • Bovine viral diarrhoea virus • Pasteurella multodda (Haemorrhagic • Capripoxvirus septicaemia) • Classical swine fever virus • Salmonella abortus oris • Crimean Congo haemorrhagic fever virus • Salmonella Gallinarum-Pullomm • Duck adenovirus A (Egg drop syndrome) • Duck hepatitis virus Other • Duck virus enteritis virus • The agent of bovine spongiform • Foot and mouth disease virus encephalopathy • Infectious bursal disease virus • Neospora caninum • Newcastle disease virus • E chinococcus granulosus • Nipah virus • Taenia spp. (T. oris, T. saginata, and T. solium) • Peste des petits ruminants virus • Trichinella spp. • Porcine epidemic diarrhoea vims

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Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 7. AFRICAN SWINE FEVER VIRUS

7.1. HAZARD IDENTIFICATION 7.1.1. Aetiological agent 7.1.3. European Union status

Family: Asfviridae, Genus: Asfvirus, Species: African Table 3 (below) summarises the ASF status of the 28 swine fever virus (ASFV) (Sánchez-Vizcaíno 2006). countries of the European Union based on their official returns to the OIE. With the exception of 7.1.2. Iceland status Sardinia (Italy), all European Union members are free of ASF (OIE 2013). The European Commission decision 2005/362/EC has approved an eradication African swine fever (ASF) has never been reported in plan for ASF in Sardinia. ASF is not recognised in Iceland and is listed as a group A notifiable disease in any of the official European Union candidate Act No 25/1993 (Willeberg 2013). Ongoing freedom countries or in any of the recognised potential is supported by general surveillance (OIE 2013). candidate countries (OIE 2013). However, ASF is now spreading through Russia, the Ukraine, and neighbouring countries in the Caucasus (Callaway 2012) and is recognised as a potential source of possible incursions into the European Union (Anonymous 2009).

Table 3: Status of African swine fever in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Has never occurred Belgium Freedom Last reported May 1985 Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Last reported 1974 Germany Freedom Has never occurred Greece Freedom Has never occurred Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Present Restricted to certain zones Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Last reported 1978 Netherlands Freedom Last reported April 1986 Poland Freedom Has never occurred Portugal Freedom Last reported November 1999 Romania Freedom Has never occurred Slovakia Freedom Has never occurred Slovenia Freedom Has never occurred Spain Freedom Last reported September 1994 Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 7.1.4. Epidemiology ASFV may be found in all tissues and body fluids of infected animals, but particularly high titres are found in the blood. ASF is often spread to new areas when The virus is not zoonotic and only infects members domestic pigs are fed uncooked or minimally cooked of the pig family (Suidae). Infections are subclinical in scraps that contain ASFV-infected pork. ASFV warthogs, bush pigs, and giant forest pigs. These remains infectious for 3-6 months in un-cooked species are the reservoir for the virus in Africa. In products such as sausages, fillets, and dry hams domesticated pigs, feral pigs, and European wild (Kleiboeker 2008). The international spread of ASF boars, infection results in clinical disease of varying has invariably been linked to the feeding to pigs of severity. There is no treatment or vaccine (Penrith et waste food containing scraps of uncooked pigmeat al. 2004). originating in countries where ASF is endemic (MacDiarmid 1991). When initially described, ASF infection of domestic pigs caused morbidity rates up to 100% and mortality Farez and Morley (1997) reviewed the survival of rates often over 90%. However, where the disease ASFV in pork and pork products and concluded that has become enzootic, a decrease in virulence may be virus may persist for up to 104 days in frozen meat or seen resulting in fatality rates as low as 2-3% (Mebus chilled meat; for up to140 days in Iberian hams 1988). including shoulder hams; for up to 140 days in white Serrano hams; for up to 399 days in Parma hams; and ASFV strains vary greatly in their virulence. Highly for up to 30 days in either pepperoni or salami virulent strains cause acute disease in naïve sausage. domesticated pigs, with the entire herd affected within days, characterised by sudden deaths with near 100% mortality. Typically, individuals present with 7.1.5. Hazard identification conclusion high fever, erythema, cyanotic skin blotching, abdominal pain, and recumbency. The virus is Although subject to an eradication plan, ASF is associated with red blood cells and macrophages, and present in the European Union. ASFV is recognised viral replication leads to thrombocytopaenia and to persist in pig meat and pig meat products for a bleeding in the skin and internal organs. Bloody significant period of time. Therefore, ASFV is diarrhoea may also be seen and pregnant animals identified as a potential hazard in pig meat and pig frequently abort (Penrith et al. 2004; Center for Food meat products imported from the EU. Safety and Public Health 2010). Animals that recover may develop persistent infections and act as virus 7.2. RISK ASSESSMENT carriers, especially African wild swine and domestic pigs in enzootic areas (OIE 2009). 7.2.1. Entry assessment

In African countries, ASF is maintained in a Pigs infected with low virulence virulent strains and subclinically infected wild pig population and individuals that have recovered from infection to transmitted to domestic pigs via the argasid tick become chronic carriers pose the greatest risk of Ornithodoros moubata, although other tick vectors (O. being infectious at slaughter and having contaminated savignyi and O. porcinus porcinus) have also been meat and products containing meat produced from described (Mebus 1988; Kleiboeker et al. 1998; them. Such individuals may not be reliably detected Kleiboeker et al. 1999; Burrage et al. 2004). In at ante-mortem and post-mortem inspection. Europe, the soft tick O. erraticus is recognised as the vector of ASFV (Wilkinson 1984) and it is thought ASVF is likely to remain infectious for 150 days in that most Ornithodoros spp. of ticks that will feed on boned meat stored at 4°C, 140 days in salted dry pigs are capable of acting as vectors for ASFV hams and several years in frozen carcasses. ASFV (Radostits et al. 2007). remains infectious for 3-6 months in un-cooked products such as sausages and fillets (Kleiboeker Once infection is established in domestic pigs, it can 2008; OIE 2009; Center for Food Security and Public spread rapidly between pigs by direct or indirect Health 2010). contact. ASFV is present in a high titre in nasopharyngeal secretions at the onset of clinical The likelihood of entry of ASFV in pig meat signs, and can be recovered from all organs of acutely imported from the European Union is assessed to be sick pigs (Radostits et al. 2007). non-negligible.

Viraemia develops within 48 to 72 hours of infection, 7.2.2. Exposure assessment and infectivity then persists for at least 7 days. The effect of the virus on haemostasis and on the vascular The primary method of spread into previously ASFV- endothelium usually results in death due to oedema free countries is thought to be through feeding and haemorrhage (Rodríguez et al. 1996; Takamatsu et uncooked or minimally cooked garbage containing al. 1999; Vallée et al. 2001).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union ASFV infected pork products to domestic pigs The increasing trend in keeping small herds of pigs in (Kleiboeker 2008). Iceland has been largely driven by the domestic industry’s desire to increase the visibility of this Although there are a small number of commercial pig species in Iceland and raise consumer awareness of farms in Iceland, there has been an increase in the food production. It would therefore be reasonable to number of people keeping a small number of pigs as conclude that there is more connectivity between a ‘hobby’. In addition there has been an increase in these hobby herds and the commercial industry in the number of sheep or cattle farms that keep a small Iceland than may be seen in other countries. An herd of pigs. Although it is unlikely that commercial outbreak of ASF in a small pig herd in Iceland is pig farms in Iceland would use kitchen waste as a therefore likely to result in spread to commercial source of feed, it is highly likely that kitchen waste herds, resulting in high mortality and an attempts to would be used as an inexpensive source of feed for eradicate disease, most likely through culling. pigs in small hobby herds. The virus infects pigs only. There would be no The likelihood of exposure is therefore assessed to be consequences for any other animals and there is no non-negligible. human health threat.

7.2.3. Consequence assessment The consequences of introduction are therefore assessed to be non-negligible.

Severity of disease seen in infected individuals would be dependent on the virulence and pathogenicity of 7.2.4. Risk estimation the introduced strain. There is no effective treatment or vaccine and a highly virulent and pathogenic strain Since entry, exposure, and consequence assessments introduced to a naïve herd is likely to result in nearly are non-negligible, the risk estimation is non- 100% mortality. negligible and ASFV is classified as a risk in unrestricted pig meat imports from the European Union.

References

Anonymous (2009). IAH warns of African swine Kleiboeker SB, Burrage TG, Scoles GA, Fish D fever threat to British pigs. Veterinary Record 165, 638­ and Rock DL (1998). African swine fever virus 639. infection in the Argasid host, Ornithodorus porcinus porcinus. Journal of Virology 72, 1711-1124. Burrage TG, Lu Z, Neilan JG, Rock Dl and Zsak L (2004). African swine fever virus multigene family Kleiboeker SB, Scoles GA, Burrage TG, Sur J-H 360 genes affect virus replication and generalization (1999). African swine fever virus replication in the of infection in Ornithodoros porcinus ticks. Journal o f midgut epithelium is required for infection of Virology 78, 2445-2453. Ornithodoros ticks. Journal of Virology 73, 8587-8598.

Callaway E (2012). Pig fever sweeps across Russia. MacDiarmid SC (1991). The importation into New Nature 488, 565-566. Zealand of meat and meat products. A review of the risks to animal health. Ministry of Agriculture and Center for Food Safety and Public Health (2010). Fisheries New Zealand, Wellington, New Zealand. African swine fever. Available at: Available at: http://www.cfsph.iastate.edu/DiseaseInfo/disease.p http: / / www.biosecurity.govt.nz / files / regs / imports / r hp?name=african-swine-fever&lang=en, last accessed isk/meat-meat-products-ra.pdf, last accessed 2 23 July 2013. September 2013.

Farez S and Morley RS (1997). Potential animal Mebus CA (1988). African swine fever. Advances in health hazards of pork and pork products. Revue Virus Research 35, 251-269. Scientifique et Technique Office International des Épigooties 16, 65-78. OIE (2009). African swine fever. Technical Disease Card. Available at: http: //www.oie.int/en/animal- Kleiboeker SB (2008). African swine fever. In: health-in-the-world/technical-disease-cards /, last United States Animal Health Association (ed.) Foreign accessed 23 July 2013. Animal Diseases. Boca Publications Group, Boca Raton. Pp. 111-116.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union OIE (2013). World Animal Health Information Takamatsu H, Denyer MS, Oura C, Childerstone Database (WAHID) Interface. Available at: A, Andersen JK, Pullen L and Parkhouse RME http: / /www.oie.int/wahis 2/public/wahid.php/Wah (1999). African swine fever virus: a B cell-mitogenic idhome/Home, last accessed 1 July 2103. virus in vivo and in vitro. Journal o f General Virology 80, 1453-1461. Penrith ML, Thompson GR and Bastos ADS (2004). African swine fever. In: Coetzer JAW, Tustin Vallée I, Tait SWG and Powell PP (2001). African RC (eds.) Infectious Diseases o f Livestock. Oxford swine fever virus infection of porcine aortic University Press, Cape Town. Pp. 1088-1122. endothelial cells leads to inhibition of inflammatory responses, activation of the thrombotic state, and Radostits OM, Gay CC, Hinchcliff KW and apoptosis. Journal of Virology 75, 10372-10382. Constable PD (2007). African swine fever (African pig disease, wart hog disease). In: Veterinary Medicine Wilkinson PJ (1984). The persistence of African 10th Edition, Saunders Elsevier. Pp. 1167-1173. swine fever in Africa and the Mediterranean. Preventive Veterinary Medicine 2, 71-82. Rodríguez F, Fernández A, Pérez J, Marín de las Mulas J, Sierra MA and Jover A (1996). African W illeberg P (2013). Chapter 5. Notification and swine fever: morphopathology of a viral animal disease surveillance. In: Risk assessments haemorrhagic disease. Veterinary Record 139, 249-254. regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Sánchez-Vizcaíno JM (2006). African swine fever. Iceland. Pp 59-90. In: Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ (eds), Diseases of Swine. 9th edition. Blackwell Publishing, Ames, Iowa. Pp. 291-307.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 8. AUJESZKY’S DISEASE VIRUS

8.1. HAZARD IDENTIFICATION 8.1.1. Aetiological agent 8.1.2. Iceland status

Family: Herpesviridae, Subfamily: Alphaherpesvirinae, Aujeszky’s disease (AD) has never been reported in Genus: Varicellovirus, Species: Suid herpesvirus 1, Iceland and is listed as a group A notifiable disease in Aujeszky’s disease virus (ADV) (Mocsari et al. 1989; Act No 25/1993 (Willeberg 2013). Ongoing freedom Davison et al. 2005). is supported by general surveillance (OIE 2013) and sporadic serological surveys since 1994 (Willeberg 2013).

8.1.3. European Union status

Table 4 (below) summarises the AD status of the 28 countries of the European Union based on their official returns to the OIE.

Table 4: Status of Aujeszky’s disease in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Freedom Last reported 1996 Belgium Present Infection in one or more zones Bulgaria Freedom Last reported January 2007 C roatia Present Demonstrated clinical disease Cyprus Freedom Last reported 1967 Czech Republic Freedom Last reported 2004 Denmark Freedom Last reported 1991 Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Last reported November 2010 Germany Freedom Last reported June 2011 Greece Freedom Last reported 2001 Hungary Present Restricted to certain zones Ireland Freedom Last reported November 2010 Italy Present Restricted to certain zones Latvia Present No clinical disease Lithuania Freedom Last reported 1988 Luxembourg Present No clinical disease Malta Freedom Has never occurred Netherlands Freedom Last reported 2004 Poland Present No clinical disease Portugal Present No clinical disease R om ania Present Demonstrated clinical disease Slovakia Freedom Last reported June 2011 Slovenia Present No clinical disease Spain Present Restricted to certain zones Sweden Freedom Last reported 1995 United Kingdom Freedom Last reported December 2009

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 8.1.4. Epidemiology Following experimental infection, the primary sites of virus replication are in the nervous tissues and lymph nodes of the head and neck (Donaldson et al. 1983). Aujeszky’s disease virus (ADV) can infect most ADV can also be isolated from lung, liver, and mammals (except primates), although infection of spleen. However, virus is not isolated from any animals other than pigs results in a fatal neurological muscle tissues. Donaldson et al. (1983) concluded disease and death within 1-3 days (Banks et al. 1999). that pigs killed 22 days after infection had virus only The pig is the only reservoir host, and all other in their tonsils and removing the head would prevent animals are dead-end hosts (Pejsak and Truszczynski transmission of ADV. Subsequently, Donaldson et al. 2006). (1984) tried to transmit ADV to recipient pigs by feeding them infective tissues (a homogenised Following infection, the incubation period ranges preparation of tonsil, masseter muscle, parotid and from 1 to 11 days (Pejsak and Truszczynski 2006). mandibular lymph nodes). Consumption did not lead Many infections are subclinical although respiratory to clinical signs or seroconversion in any recipients. and nervous signs may be seen with high mortality in young pigs. Beran (1991) concluded that the likely source of infection of pig herds in the United States during Piglets may die without showing clinical signs. 1990 was rarely attributable to contact with Weaned pigs show respiratory illness but recover, and contaminated carcasses of infected swine. Banks et al. infection in adult pigs is generally inapparent or (1999) reported the death of several circus bears results in mild respiratory signs. Abortion, stillbirths, resulting from the consumption of pig heads certified and sporadic cases with neurological signs may also as fit for human consumption. occur in adults (Donaldson et al. 1983; Center for Food Security and Public Health 2006). ADV is Consistent with these reports, the OIE Code describes found in nasal secretions and is transmitted by direct fresh meat of domestic and wild pigs not containing nose-to-nose contact or over short distances by offal (head, and thoracic and abdominal viscera), aerosols (Van Oirschot 2004). meat products of domestic and wild pigs not containing offal (head, and thoracic and abdominal Virus is excreted from infected pigs before the onset viscera), and products of animal origin not containing of clinical signs and continues for up to three weeks offal (head, and thoracic and abdominal viscera) as after infection. Most pigs that recover from infection ‘safe commodities’ (OIE 2013b). become latent carriers with viral DNA present in trigeminal ganglia (Pejsaket and Truszczynski 2006). However, reactivation and subsequent viral excretion 8.1.5. Hazard identification conclusion is rare, appearing not to play an important role in the epidemiology of the disease (Van Oirschot 2004). Aujeszky’s disease is present in a number of European Union counties. ADV is unlikely to be Cases of AD in dogs, cats, farmed mink and ferrets, associated with pig meat although may be present in and wild rats have been attributed to the eating of commodities containing pig offal (head, and thoracic meat from AD infected swine. Outbreaks in pigs and abdominal viscera). have been attributed to their eating the carcasses of rats dying of the disease. While it is possible that pigs However, as noted in the commodity definition can be infected via pork scraps the lack of (Section 4), offal is exclude from the scope of this prominence given this possibility by most writers risk assessment. Therefore, ADV is not identified as suggests that it is not very probable (MacDiarmid a hazard in unrestricted meat imports from the 1991). European Union.

References

Banks M, Monsalve Torraca AG, Greenwood AG Center for Food Security and Public Health and Taylor DC (1999). Aujeszky’s disease in captive (2006). Aujeszky’s disease. Available at: bears. Veterinary Record 145, 362-365. http://www.cfsph.iastate.edu/DiseaseInfo/disease.p hp?name=aujeszkys-disease&lang=en. last accessed Beran GW (1991). Transmission of Aujeszky’s 31 July 2013. disease virus. First International Symposium on Eradication of Pseudorabies (Aujeszky’s) Virus. St. Paul, Minnesota, University of Minnesota, College of Veterinary Medicine.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Davison AJ, Eberle R, Hayward GS, McGeogh OIE (2013a). World Animal Health Information DJ, Minson AC, Pellett PE, Roizman B, Studdert Database (WAHID) Interface. Available at: MJ and Thirly E (2005). Genus Variocellovirus. In: http://www.oie.int/wahis 2/public/wahid.php/Wah Fauquet CM, Mayo MA, Maniloff J, Desselberger U, idhome/Home, last accessed 1 July 2103. Ball LA (eds), Eighth Report o f the International Committee on Taxonomy of Viruses. Elsevier Academic Press, OIE (2013b). Chapter 8.2. Infection with Aujeszky’s Amsterdam. Pp. 200-201. disease virus. In OIE Terrestrial Animal Health Code, OIE, Paris, Available at: Donaldson AI, Wardley RC, Martin S and Ferris http://www.oie.int/index.php?id=169&L=0&htmfil NP (1983). Experimental Aujeszky’s disease in pigs: e=chapitre 1.8.2.htm, last accessed 31 July 2013. Excretion, survival and transmission of the virus. Veterinary Record 113, 490-494. Pejsak ZK and Truszczynski MJ (2006). Aujeszky's disease (pseudorabies). In: Straw BE, Donaldson AI, Wardley RC, Martin S and Zimmerman JJ, D'Allaire S, Taylor DJ (eds), Diseases Harkness JW (1984). Influence of vaccination on o f Swine. 9th edition, Blackwell Publishing, Ames, Aujeszky’s disease virus and disease transmission. Iowa. Pp. 419-433. Veterinary Record 115, 121-124. Van Oirschot JT (2004). Pseudorabies. In: Coetzer MacDiarmid SC (1991). The importation into New JAW, Tustin RC (eds), Infectious Diseases of Livestock. Zealand of meat and meat products. A review of the Vol. 2, Oxford University Press, CapeTown. Pp. 909­ risks to animal health. Ministry of Agriculture and 922. Fisheries New Zealand, Wellington, New Zealand. Available at: W illeberg P (2013). Chapter 5. Notification and http: / / www.biosecurity.govt.nz/ files / regs/imports / r animal disease surveillance. In: Risk assessments isk/meat-meat-products-ra.pdf, last accessed 2 regarding open trade in live animals to Iceland. Icelandic September 2013. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp 59-90. Mocsari E, Szolnoki J, Glavits R and Zsak L (1989). Horizontal transmission of Aujeszky's disease virus from sheep to pigs. Veterinary Microbiology 19, 245-252.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 9. AVIAN ENCEPHALOMYELITIS VIRUS

9.1. HAZARD IDENTIFICATION 9.1.1. Aetiological agent Infection of young chickens leads to paralysis whilst infection of older birds may be subclinical with effects on egg production and hatchability (Jungherr Member of the Family Picornaviridae, Genus and Minard 1942; Taylor et al. 1955). AEV primarily Tremovirus. Avian encephalomyelitis virus (AEV) (Marvil et infects chickens although disease has also been al 1999). reported in turkeys and quail (Tannock and Shafren 1994). 9.1.2. Iceland status Vertical and horizontal transmission of AEV is Avian encephalomyelitis is a notifiable disease, recognised although infection via the oral-faecal route according to Act No 25/1993. Clinical disease has is considered most important (Tannock and Shafren never been detected. Samples have been taken 1994). Following oral infection, virus multiplies in occasionally since 1993 (Willeberg 2013). the intestinal epithelium and can be recovered from faeces within three days of inoculation (Calneck et al. 9.1.3. European Union status 1961). Following multiplication, virus spreads to the pancreas, liver, and spleen before subsequently infecting the central nervous system (Springer and Outbreaks of disease have been reported throughout Schmittle 1968; Ikeda et al. 1976a; Ikeda et al. 1976b). the world including the United States, Canada, Japan, There is no evidence to indicate AEV may be Australia, and Europe (Tannock and Shafren 1994). recovered from the meat of infected birds or that AEV has been spread internationally through trade in 9.1.4. Epidemiology poultry meat.

Following the initial identification of avian 9.1.5. Hazard identification conclusion encephalomyelitis in the United States in 1930 (Jones 1932), the disease spread rapidly throughout North As there is no evidence to suggest the virus is likely to America by 1950 (Taylor and Schelling 1960). be recovered from the meat of infected birds, AEV is not identified as a hazard in unrestricted meat imports from the European Union.

References

Calneck BW, Taylor PJ and Sevoian M (1961). Marvil P, Knowles NJ, Mockett AP, Britton P, Studies on avian encephalomyelitis. V Development Brown TD and Cavanagh D (1999). Avian and application of an oral vaccine. Avian Diseases 5, encephalomyelitis virus is a picornavirus and is most 297-312. closely related to hepatitis A virus. Journal of General Virology 80, 653-662. Ikeda S, Matsuda K and Yonaiyama K (1976a). Susceptibility of chickens to avian encephalomyelitis Springer WT and Schmittle SC (1968). Avian virus. I Behaviour of the virus in day-old chicks. encephalomyelitis. A chronological study of the National Institute o f Animal Health Quarterly 16, 1-7. histopathogenesis in selected tissues. Avian Diseases 12, 229-239. Ikeda S, Matsuda K and Yonaiyama K (1976b). Susceptibility of chickens to avian encephalomyelitis Tannock GA and Shafren DR (1994). Avian virus. III Behaviour of the virus in growing chicks. encephalomyelitis: A review. Avian Pathology 23, 603­ National Institute o f Animal Health Quarterly, 16, 33-38. 620.

Jones EE (1932). An encephalomyelitis in the Taylor JRE and Schelling EP (1960). The chicken. Science 76, 331-332. distribution of avian encephalomyelitis in North America as indicated by an immunity test. Avian Jungherr E and Minard EL (1942). The present Diseases 4, 122-133. status of avian encephalomyelitis. Journal of the American Veterinary Medical Association 100, 38-46.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Taylor LW, Lowry DC and Raggi LG (1955). W illeberg P (2013). Chapter 5. Notification and Effects of an outbreak of avian encephalomyelitis animal disease surveillance. In: Risk assessments (epidemic tremor) in a breeding flock. Poultry Science regarding open trade in live animals to Iceland. Icelandic 34, 1036-1045. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 10. AVIAN INFECTIOUS BRONCHITIS VIRUS

10.1. HAZARD IDENTIFICATION 10.1.1. Aetiological agent 10.1.2. Iceland status

Family Coronaviridae; Genus Coronavirus; Species Avian Avian infectious bronchitis (IB) was frequently Infectious Bronchitis Virus (IBV). detected in Iceland between 1995 and 2002 although serological surveys in 2010, 2011, and 2012 returned IBV does not constitute a single homogenous no positive results. IB is listed as a group B notifiable antigenic type. The prototype virus is Massachusetts disease in Act No 25/1993 (Willeberg 2013). There M41 but a plethora of IBV strains exist and new IBV is general and targeted surveillance for this disease variants continue to be recognised (Dhinakar Raj and (OIE 2013). Jones 1997; Cook 2008). 10.1.3. European Union status

Table 5 (below) summarises the IB status of the 28 countries of the European Union based on their official returns to the OIE.

Table 5: Status of avian infectious bronchitis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last reported 2004 Bulgaria Not reported Croatia Freedom Date of last occurrence unknown Cyprus Freedom Last reported 2004 Czech Republic Freedom Last reported 2004 Denmark Present Disease suspected Estonia Freedom Date of last occurrence unknown Finland Present Clinical disease France Freedom Date of last occurrence unknown Germany Freedom Last reported December 2008 Greece Freedom Last reported 2002 Hungary Present Disease restricted to certain zones Ireland Present Clinical disease Italy Freedom Date of last occurrence unknown Latvia Freedom Has never occurred Lithuania Freedom Date of last occurrence unknown Luxembourg Freedom Date of last occurrence unknown Malta Freedom Last reported December 2008 Netherlands Present Clinical disease Poland Not reported Portugal Present Clinical disease Romania Freedom Date of last occurrence unknown Slovakia Freedom Last reported 2000 Slovenia Freedom Last reported June 2009 Spain Present Clinical disease Sweden Freedom Last reported 2008 United Kingdom Present Clinical disease

10.1.4. Epidemiology seen between strains from different geographic regions (McMartin 1993; McFarlane and Verma 2008). Avian IB is predominantly a respiratory IBVs are ubiquitous where poultry are reared infection, however three clinical manifestations of intensively (Wit et al. 2010) and extensive antigenic IBV infection are observed in the field; respiratory variation and differences in virulence and tropism is

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union disease, reproductive disorders, and nephritis oviduct can lead to permanent damage in immature (Ignjatovic and Sapats 2000). birds and a drop in egg production (exceeding 50%) and quality in hens. There are also reports of variant IBV primarily infects chickens but other avian species strains causing pectoral myopathy (Dhinakar Raj and (racing pigeons, guineafowl, partridge, peafowl, and Jones 1997) and proventriculitis (Benyeda et al. 2010). teal) have also been reported to be infected with IBV- The QX strain of IBV has been associated with a like viruses (Barr et al. 1988; Ito et al. 1991; Cavanagh wide range of clinical problems including respiratory 2005; Liu et al. 2005). These cases were not disease, wet litter, mortality due to kidney damage, associated with disease but the isolated viruses were proventriculitis, and decreased flock performance. able to infect and cause disease when inoculated into Infection of layers with the QX strain has been chickens. The capacity of IBV to replicate in other associated with ‘blind’ or ‘false-layer’ syndrome due avian hosts without causing overt disease raises to oviduct lesions (Irvine et al. 2010). potential for these birds to carry and transmit the virus although there is no evidence that this can Latent infection (from both vaccine and field strains) occur under field conditions. There are no recorded can establish in the kidney and caecal tonsils for up to cases of natural infection of commercial turkeys or 163 days or longer, with subsequent erratic shedding ducks with IBV (Cavanagh 2005). of virus via both faeces and aerosol (Ignjatovic and Sapats 2000; Cavanagh and Gelb 2008) and often IBV is highly infectious to chickens of all ages, and with long pauses (up to 42 days) between episodes of under natural conditions will spread between houses shedding (Naqi et al. 2003). Virus re-excretion is not within 1 to 2 days, and between farms within 3 to 4 generally accompanied by clinical signs and may serve days (Ignjatovic and Sapats 2000). as a source of infection to susceptible chickens (Dhinakar Raj and Jones 1997). The virus is present in considerable titres in tracheal mucus and faeces during the acute and recovery 10.1.5. Hazard identification conclusion phases of disease, respectively. The virus may be shed for more than 20 weeks after clinical recovery IB viruses are found in a number of European Union and can persist in the intestinal tract for several countries and can be recovered from tissues of the months (Alexander and Gough 1977; Cook 2008). respiratory, digestive, reproductive, and urinary Spread occurs horizontally by aerosol or by ingestion systems of infected chickens. There are no reports of of faeces or contaminated feed or water. The most IBV being found in muscle. IBV is not identified as a common source of infection is direct chicken-to- hazard in poultry meat or meat products. chicken contact, but indirect transmission via mechanical spread, sometimes over long distances, There are no reports of natural or experimental IBV also occurs (Gelb 2008). The virus can survive for a infection in commercial turkeys or ducks. However, considerable time in faeces. True egg transmission is chickens infected with IBV may not show gross believed to be insignificant. pathological lesions that would prompt removal from the processing line. Additionally prolonged shedding The upper respiratory tract is the initial site of IBV of IBV can occur following recovery from clinical replication, regardless of strain, following which a disease and the trachea, lungs, bursa of Fabricius, and viraemia occurs, disseminating the virus to other kidney are recognised as sources of virus (Naqi et al. epithelial surfaces, including the kidney, oviduct, 2003). IBV is identified as a potential hazard in testes, bursa of Fabricius, and alimentary tract imported chicken meat products that may contain (McMartin 1993; Cavanagh 2007). fragments of these tissues (such as whole chicken carcases). Respiratory signs are the first and most common clinical manifestation in birds of all ages and include 10.2. RISK ASSESSMENT tracheal rales, gasping, sneezing, and watery nasal 10.2.1. Entry assessment discharge (Cook 2008). In uncomplicated cases these signs are short-lived (10—14 days) and mortalities are generally low. Frequently infection is complicated by Circumstantial evidence indicates that unrestricted secondary infections with organisms such as trade in poultry products has contributed to the infectious bursal disease virus, Mycoplasma gallisepticum, spread of some IBV serotypes (Ignjatovic and Sapats or Escherichia coli. IBV interacts synergistically with 2000). Fragments of infective tissues present in these organisms and co-infection is considered the poultry carcases after processing may be a source of main cause of mortality in older birds (Lopez and IBV and chickens of slaughter age are susceptible to McFarlane 2006; Cavanagh 2007). infection. The likelihood of entry of IBV in imported whole chicken carcases is assessed to be non- Nephropathogenic IBV (NIBV) strains initially cause negligible. some respiratory signs followed by signs due to kidney damage and mortalities up to 30% (Ignjatovic and Sapats 2000; Cook 2008). Infection of the

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 10.2.2. Exposure assessment described above, the likelihood that IBV would infect a wild bird consuming contaminated meat scraps is extremely low. It is therefore concluded that there is There are a small number of large commercial poultry a negligible likelihood of commercial poultry being flocks in Iceland and currently no commercial free­ exposed to IBV. range poultry farms. Backyard poultry keeping in Iceland is becoming increasingly popular and official data indicates over 403 poultry flocks in Iceland with 10.2.3. Consequence assessment <100 hens. Although waste food would not be used as feed in Iceland’s commercial poultry flocks, it is In its virulent respiratory forms, IBV is considered very likely that waste food from domestic kitchens or the most rapidly spreading virus known in birds bakeries might be used to feed small backyard poultry (McMartin 1993). In the United Kingdom and the flocks. Most strains of IBV are inactivated after 15 United States of America IBV is the most significant minutes at 56°C and after 90 minutes at 45°C source of economic loss to the broiler industry (Cavanagh and Gelb 2008). There is considered to be despite the extensive use of vaccines (Ignjatovic and a negligible likelihood of backyard poultry flocks Sapats 2000; Cavanagh 2007). IBV is highly being exposed to IBV from scraps of cooked whole contagious and is able to spread very rapidly in non­ chicken carcases. IBV can be readily transmitted by protected birds (Wit et al. 2010). The consequence of the oral route and there is a non-negligible likelihood IBV infection depends on many factors, including the of exposure to IBV from feeding raw scraps strain of virus, age and breed of chicken, nutrition, generated during the domestic processing of environment, and intercurrent infections. Most imported whole chicken carcases. exotic strains result in an acute, highly infectious respiratory disease of chickens, affecting egg Evidence suggests that IBV is able to infect and production and quality in laying hens, production replicate in a wide range of avian species without performance in broilers, and mortalities associated causing overt disease. Additionally it is known that with secondary infections. However, as described the virus has a long outdoor survival time in cool above, even if IBV were to be introduced into a small climates. The oral dose of IBV sufficient to initiate backyard poultry flock in Iceland, any consequences infection in wild birds is not known. However, the would be limited to that small flock and there is a likelihood of free-living avian species being infected negligible likelihood of disease spreading to a with IBV, either following exposure to an infected commercial flock due to the high biosecurity backyard chicken flock, or through consumption of standards that are in place in Iceland. kitchen waste disposed of at sites accessible to susceptible wild avian species, is assessed to be Although IBV potentially has a wide host range, extremely low. disease has only been documented in the chicken and the consequences in other bird species are considered Commercial poultry farms in Iceland are unlikely to negligible. Non-avian species are not susceptible to feed waste food and there are no commercial free­ infection with IBV. range poultry flocks in Iceland. Commercial poultry flocks in Iceland have a high standard of biosecurity The consequence assessment is therefore negligible. and there is a negligible likelihood of significant contact between commercial flocks and backyard flocks. Infection of wild birds with IBV, with 10.2.4. Risk estimation subsequent spread to commercial poultry, has never been reported and the only evidence that wild birds As the consequence assessment is negligible, the risk are able to transmit IBV infection to chickens has estimate is negligible and IBV is not assessed to be a been experimental. There are no reports implicating risk in unrestricted meat imports from the European wild birds in the epidemiology of IBV and as Union.

References

Alexander DJ and Gough RE (1977). Isolation of Benyeda Zs, Szeredi L, Mato T, Suveges T, avian infectious bronchitis virus from experimentally Balka Gy, Abony-Toth Zs, Rusvai M and Palya V infected chickens. Research in Veterinary Science 23, (2010). Comparative histopathology and 344-347. immunohistochemistry of QX-like, Massachusetts and 793/B serotypes of infectious bronchitis virus Barr DA, Reece RL, O’Rourke D, Button C and infection in chickens. Journal of Comparative Pathology Faragher JT (1988). Isolation of infectious 143, 276-283. bronchitis virus from a flock of racing pigeons. Australian Veterinary Journal 65, 228. Cavanagh D (2005). Coronaviruses in poultry and other birds. Avian Pathology 34, 439-448.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Cavanagh D (2007). Coronavirus avian infectious Liu S, Chen J, Chen J, Kong X, Shao Y, Han Z, bronchitis virus. Veterinary Research 38, 281-297. Feng L, Cai X, Gu S and Liu M (2005). Isolation of avian infectious bronchitis coronavirus from Cavanagh D and Gelb JJr (2008). Infectious domestic peafowl (Pavo cristatus) and teal {Anas). Bronchitis. In Diseases o f Poultry 12th Edition. Eds Journal of General Virology 86, 719-725. Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan LK and Swayne DE, Blackwell Publishing. Pp. Lopez JC and McFarlane R (2006). 511-526. Environmental factors influence the prevalence of infectious bronchitis virus. Proceedings o f the 18th Cook J (2008). Coronaviridae. In Poultry Diseases 6th Australian Poultry Science Symposium, Sydney, New Edition, Eds Pattison M, McMullin PF, Bradbury JM South Wales, Australia, 127-130. and Alexander DJ, Elsevier/Butterworth-Heinemann. Pp. 340-349. McFarlane R and Verma R (2008). Sequence analysis of the gene coding for the S1 glycoprotein of Dhinakar Raj G and Jones RC (1997). Infectious infectious bronchitis virus (IBV) strains from New bronchitis virus: immunopathogenesis of infection in Zealand. Virus Genes 37, 351-357. the chicken. Avian Pathology 26, 677-706. McMartin D (1993). Infectious Bronchitis. In Virus Gelb J (2008). Chapter 2.3.2. Avian infectious Infections o f Birds, Volume 4, Eds McFerran JB and bronchitis. In: OIE Manual of Diagnostic Tests and McNulty MS, Elsevier Science Publishers BV. Pp. Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: 249-274. http://www.oie.int/fileadmin/Home/eng/Health st andards/tahm/2.03.02 AIB.pdf, last accessed 1 July Naqi S, Gay K, Patalla P, Mondal S and Liu R 2013. (2003). Establishment of persistent avian infectious bronchitis virus infection in antibody-free and Ignjatovic J and Sapats S (2000). Avian infectious antibody-positive chickens. Avian Diseases 47, 594­ bronchitis virus. Revue Scientifique et Technique Office 601. International des Épiyooties 19, 493-508. OIE (2013). World Animal Health Information Irvine RM, Cox WJ, Ceeraz V, Reid SM, Ellis RJ, Database (WAHID) Interface. Available at: Jones RM, Errington J, Wood AM, McVicar CM http://www.oie.int/wahis 2/public/wahid.php/Wah and Clark MI (2010). Detection of IBV QX in idhome/Home, last accessed 1 July 2103. commercial broiler flocks in the UK. Veterinary Record 167, 877-879. W illeberg P (2013). Chapter 5. Notification and animal disease surveillance. In: Risk assessments Ito NMK, Miyaji CI and Capellaro CEMPDM regarding open trade in live animals to Iceland. Icelandic (1991). Studies on broiler’s IBV and IB-like virus Food and Veterinary Authority (MAST), Reykjavik, from guinea fowl. In Second International Symposium on Iceland. Pp 59-90. Infectious Bronchitis, Eds Kalata EF and Heffels- Redmann U, Giessen, Germany, Justus Leibig Wit JJ (Sjaak) de, Cook JKA and van der Heijden University, 302-307. HMJF (2010). Infectious bronchitis virus in Asia, Africa, Australia and Latin America - History, current situation and control measures. Bragiüan Journal of Poultry Science 12, 97-106.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 11. AVIAN INFLUENZA VIRUS

11.1. HAZARD IDENTIFICATION 11.1.1. Aetiological agent 11.1.2. Iceland status

Family: Orthomyxoviridae, Genus: Influenzavirus A Avian influenza is listed as a group A notifiable (Fauquet et al. 2005). Many strains of varying disease in Act No 25/1993. Clinical disease virulence are known. associated with avian influenza has never been described in Iceland. In domestic poultry, four H5 Influenzavirus A is subtyped based on serologic positive samples were recovered from 352 surveyed reactions to the haemagglutinin (H) and individuals in 2006 and four influenza A positive (H5 neuraminidase (N) surface glycoproteins (WHO negative) samples were recovered from 120 surveyed Expert Committee 1980). Sixteen subtypes of H and individuals in 2012. Surveys of wild bird faecal nine subtypes of N are recognised. The distribution samples returned eight positive test results (including of virus subtypes varies by year, geographic location, one H5 positive) from a total of 2549 samples and host species (Swayne and Halvorson 2008). examined between 2006 and 2010 (Willeberg 2013). There is general and targeted surveillance for these High pathogenicity avian influenza (HPAI) and low diseases (OIE 2013b). pathogenicity avian influenza (LPAI) in poultry are listed by the OIE as notifiable diseases. Article 10.4.1 11.1.3. European Union status of the current OIE Code (OIE 2013a) states that, for the purposes of international trade, avian influenza Tables 6 and 7 (below) summarises the HPAI and (AI) in its notifiable form (NAI) is defined as an LPAI status of the 28 countries of the European infection of poultry caused by any influenza A virus Union based on their official returns to the OIE. of the H5 or H7 subtypes or by any AI virus with an intravenous pathogenicity index (IVPI) greater than 1.2 (or as an alternative at least 75% mortality). NAI viruses can be divided into high pathogenicity notifiable avian influenza (HPNAI) and low pathogenicity notifiable avian influenza (LPNAI):

• HPNAI viruses have an IVPI in 6-week-old chickens greater than 1.2 or, as an alternative, cause at least 75% mortality in 4- to 8-week-old chickens infected intravenously. H5 and H7 viruses which do not have an IVPI of greater than 1.2 or cause less than 75% mortality in an intravenous lethality test should be sequenced to determine whether multiple basic amino acids are present at the cleavage site of the haemagglutinin molecule (HA0); if the amino acid motif is similar to that observed for other HPNAI isolates, the isolate being tested should be considered as HPNAI; • LPNAI are all influenza A viruses of H5 and H7 subtype that are not HPNAI viruses.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 6: Status of high pathogenicity avian influenza in European Union countries based on their official returns to the OIE (OIE 2013b)

EU M em ber Disease status O ther Austria Freedom Last reported April 2006 Belgium Freedom Last reported 2003 Bulgaria Freedom Last reported 2010 Croatia Freedom Last reported October 2006 Cyprus Freedom Has never occurred Czech Republic Freedom Last reported August 2007 Denmark Freedom Last reported May 2006 Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Last reported February 2006 Germany Freedom Last reported October 2008 Greece Freedom Last reported March 2006 Hungary Freedom Last reported 2007 Ireland Freedom Last reported 1983 Italy Freedom Last reported February 200610 Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Last reported 1956 Malta Freedom Has never occurred Netherlands Freedom Last reported 2003 Poland Freedom Last reported January 2008 Portugal Freedom Has never occurred Romania Freedom Last reported April 2010 Slovakia Freedom Last reported 2006 Slovenia Freedom Last reported March 2006 Spain Freedom Last reported October 2009 Sweden Freedom Last reported March 2006 United Kingdom Freedom Last reported August 2008

10 An outbreak of HPAI was reported by Italy on 15 August 2013 although this was reported to have been resolved by 18 September 2013.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 7: Status of low pathogenicity avian influenza in European Union countries based on their official returns to the OIE (OIE 2013b)

EU M em ber Disease status O ther Austria Freedom Last reported 2009 Belgium Freedom Last reported January 2009 Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Last reported November 2009 Denmark Present Recurrence reported 2013 Estonia Freedom Last occurrence unknown Finland Freedom Has never occurred France Present Disease suspected Germany Present Clinical disease Greece Freedom Last occurrence unknown Hungary Freedom Last occurrence unknown Ireland Present Clinical disease Italy Present Clinical disease Latvia Freedom Has never occurred Lithuania Freedom Last occurrence unknown Luxembourg Freedom Last reported 1992 Malta Freedom Has never occurred Netherlands Present Infection present in one or more zones Poland Freedom Has never occurred Portugal Freedom Last reported January 2008 Romania Freedom Last reported December 2010 Slovakia Freedom Last occurrence unknown Slovenia Freedom Last occurrence unknown Spain Freedom Last reported 2009 Sweden Freedom Has never occurred United Kingdom Freedom Last reported May 2007

11.1.4. Epidemiology al. 1995), and whales (Lvov et al. 1978; Hinshaw et al. 1986a). In a number of these reported cases, exposure to infected sea birds was suggested as the AI viruses are most frequently recorded in waterfowl most likely source of virus. HPAI has been (Webster et al. 1992; Stallknecht 1998; Perdue et al. associated with sporadic infections in mammals 2000). Wild birds, particularly migratory waterfowl, where there is close contact with or consumption of may play a major role in the initial introduction of AI infected birds (FAO 2006). viruses into commercial poultry (Halvorson et al. 1985; Hinshaw et al. 1986b) but once established in commercial poultry, wild birds have very little or no LPAI infection of domestic poultry can cause mild to role in secondary dissemination (Nettles et al. 1985). severe respiratory signs including coughing, sneezing, AI is rare in commercial integrated poultry systems in rales, rattles, and excessive lacrimation. Generalised developed countries but, when infection does occur, clinical signs such as huddling, ruffled feathers, it can spread rapidly throughout the integrated depression, lethargy, and, occasionally, diarrhoea have system, resulting in epidemics of HPAI or LPAI also been described. Layers may show decreased egg (Swayne and Halvorson 2008). production. High morbidity and low mortality is normal for LPAI infections (Swayne and Halvorson 2008). Intratracheal inoculation of poultry with LPAI Although most influenza viruses found in domestic can result in localised infection of the upper and poultry have been of avian origin, H1N1, H1N2, and lower respiratory tract (tracheitis, bronchitis, H3N2 swine influenza viruses have also been isolated airsaccultitis, and pneumonia) with histological from flocks experiencing a drop in egg production lesions and viral antigen distribution restricted to the (Mohan et al. 1981; Easterday et al. 1997; Suarez et al. lungs and trachea although pancreatic necrosis is also 2002; Tang et al. 2005). In these cases, the proximity reported (Swayne et al. 1992; Shalaby et al. 1994; Mo et of infected flocks to swine operations is consistently al. 1997; Capua et al. 2000). Intravenous inoculation suggested as the most likely source of virus. LPAI of poultry with LPAI results in swollen and mottled has been associated with epidemics of respiratory kidneys with necrosis of the renal tubules and disease in mink (Englund et al. 1986), seals (Lang et al. interstitial nephritis noted on histopathology and high 1981; Webster et al. 1981; Geraci et al. 1982; Callan et

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union viral titres in kidney tissues (Slemons and Swayne An early study found that AI virus persisted in 1990; Swayne and Slemons 1990; Slemons and refrigerated muscle tissue for 287 days although Swayne 1992; Swayne and Slemons 1992; Shalaby et feeding meat or blood from a viraemic bird to a al. 1994; Swayne and Alexander 1994; Swayne et aL susceptible bird did not transmit infection (Purchase 1994; Swayne and Slemons 1995). However, this 1931). Swayne and Beck (2005) demonstrated that renal tropism is strain-specific and is most LPAI virus could not be found in the blood, bone consistently associated with experimental intravenous marrow, breast or thigh meat of experimentally inoculation studies (Swayne and Halvorson 2008) infected poultry and that feeding breast or thigh meat although Alexander and Gough (1986) did report the to a susceptible bird did not transmit infection. recovery of H10N4 LPAI from kidneys taken from However, experimental infection of poultry with hens presenting with nephropathy and visceral gout. HPAI resulted in detectable virus in blood, bone Salpingitis associated with a non-pathogenic H7N2 marrow, and breast and thigh meat. An H5N2 isolate virus was described by Zielger et aL (1999). was found to achieve only low viral titres in muscle tissue (1022-32 EID 50 virus/g) and feeding of In contrast, most HPAI infections of domestic susceptible birds with this meat did not transmit poultry are associated with severe disease with some infection, whereas an H5N1 isolate achieved a much birds being found dead before clinical signs are higher titre in muscle tissue (1073 EID 50 virus/g) noticed. Clinical signs such as tremors, torticollis, which was sufficient to achieve transmission in a and opisthotonus may be seen for 3-7 days before feeding trial. This study also demonstrated that AI death. Precipitous drops in egg production in virus vaccination prevented HPAI virus replication in breeders and layers are reported. Morbidity and muscle tissue. The authors concluded that their data mortality are usually very high (Swayne and indicated that the potential for LPAI virus appearing Halvorson 2008). HPAI of poultry results in necrosis in the meat of infected chickens was negligible, while and inflammation of multiple organs including the the potential for having HPAI virus in meat from cloacal bursa, thymus, spleen, heart, pancreas, kidney, infected chickens was high although proper usage of brain, trachea, lung, adrenal glands, and skeletal vaccines could prevent HPAI from being present in muscle (Mo et aL 1997; Swayne 1997; Perkins and meat. Swayne 2001). Histopathological lesions described include diffuse nonsuppurative encephalitis, 11.1.5. Hazard identification conclusion necrotising pancreatitis, and necrotising myositis of skeletal muscles (Acland et aL 1984). Viral infection LPAI is reported to be present in a number of of the vascular endothelium is suggested as the European Union countries. Studies have shown that mechanism for the pathogenesis of HPAI infections LPAI cannot be transmitted to susceptible birds by in poultry, especially the central nervous system feeding meat derived from an infected bird. lesions (Kobayashi et aL 1996a; Kobayashi et aL Following natural infection, LPAI virus replication is 1996b). Viral antigen can be detected in multiple limited mainly to the respiratory tract tissues although organs, most commonly the heart, lung, kidney, brain, some infectivity might be associated with the and pancreas (Mo et aL 1997). pancreas, kidneys and reproductive tract. LPAI is not identified as a potential hazard in imports of poultry Infection of wild birds with either HPAI or LPAI meat that are free of viscera. However, LPAI is usually produces no mortality or morbidity (Swayne identified as a potential hazard in poultry meat or and Halvorson 2008) although recent H5N1 HPAI meat products that may contain remnants of viscera viruses have been associated with deaths in a number (for example, entire chicken carcases). of wild bird species in Asia (Ellis et aL 2004; Chen et al. 2005; Sims et al. 2005; Webster et al. 2005). HPAI viruses replicate in a wide range of tissues and studies have shown that feeding meat from an AI virus replicates in the respiratory, intestinal, renal, infected bird can transmit virus to a susceptible bird. and reproductive organs and virus is excreted from Although all European Union countries currently the nares, mouth, conjunctiva, and cloaca of infected report freedom from these viruses, outbreaks of birds (Swayne and Halvorson 2008). Virus HPAI are frequently reported from the European transmission is believed to occur by direct contact, Union. HPAI is identified as a potential hazard in through aerosol droplet exposure or via fomites unrestricted meat imports from the European Union. (Easterday et al. 1997). However, air sampling during the 1983-84 HPAI outbreak in the northeastern United States did not recover virus from samples 11.2. RISK ASSESSMENT taken more than 45m downwind of an infected flock, 11.2.1. Entry assessment suggesting airborne transmission is likely to be much less significant for transmission between farms than Although there is the possibility that LPAI may be mechanical movement on fomites (Brugh and associated with viscera adherent to imported poultry Johnson 1987). carcases, the likelihood of virus introduction through this route is insignificant compared to the likelihood of LPAI introduction into Iceland as a result of

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union natural bird migration. Large numbers of waterfowl poultry farms in Iceland, there is a much greater migrate through Iceland every year, for example likelihood of wild birds being exposed to HPAI from White-fronted Geese arrive in considerable numbers an infected backyard flock than from a commercial every year in the Spring and Autumn as they migrate property. between the United Kingdom and Greenland (Francis and Fox 1987). Such migratory travel is far In previous HPAI outbreaks affecting multiple more likely to introduce LPAI into Iceland (as countries, the spread of virus has been directly or illustrated in 11.1.2 above) than remnants of viscera indirectly attributable to human activity (Webster et al. in imported poultry meat from the European Union. 2005). However, more recently, infection of wild For LPAI, the likelihood of entry is assessed to be birds from poultry has been implicated in the spread negligible. of H5N1 in Asia (Chen et al. 2005; Sims et al. 2005; Webster et al. 2005). Swayne and Beck (2005) demonstrated that chicken breast meat was capable of transmitting HPAI The likelihood of free-living avian species being (H5N1) to a susceptible bird, resulting in infection infected with HPAI, either following exposure to an and death after 2 days. 80% mortality was described infected backyard flock or through consumption of in 4-week-old chickens directly fed an average of scraps of uncooked poultry meat in kitchen waste <3.5g of breast meat from an infected bird and 100% disposed of at sites accessible to susceptible wild mortality was described when the meat was added to avian species is assessed to be non-negligible. drinking water. It is therefore reasonable to conclude that the likelihood of HPAI being present in Although poultry flocks in Iceland have a generally imported poultry meat is non-negligible. high level of biosecurity and there are currently no commercial free-range poultry flocks, the 11.2.2. Exposure assessment introduction of AI viruses to commercial poultry by migratory waterfowl has been documented Cooking chicken meat to a core temperature of 70°C (Halvorson et al. 1985) so the likelihood of exposure for 5.5 seconds would be likely to achieve an 11 log of commercial poultry from free-living avian species reduction in virus titre (Thomas and Swayne 2007) so is assessed as non-negligible. Furthermore, in most domestic cooking can be considered to reliably outbreaks of AI investigated, faecal shedding creates inactivate any HPAI present in imported poultry a high concentration of virus that may persist in the meat. However, the study of Swayne and Beck environment for prolonged periods, and secondary (2005) demonstrates that small scraps of uncooked spread from an infected flock appears to follow the poultry breast meat should be considered capable of movement of people and equipment (Brugh and infecting susceptible birds so raw scraps generated Johnson 1987). during the domestic processing of imported chicken or duck meat are likely to contain sufficient virus to In conclusion, the likelihood of exposure of backyard be able to transmit infection. poultry, wild birds, and commercial poultry is assessed to be non-negligible. There are a small number of large commercial poultry flocks in Iceland and currently no commercial free­ 11.2.3. Consequence assessment range poultry farms. Backyard poultry keeping in Iceland is becoming increasingly popular and official The introduction of HPAI in domestic poultry could data indicates over 403 poultry flocks in Iceland with result in widespread disease with high mortalities <100 hens. Although waste food would not be used leading to disruption of the poultry industry. The as feed in Iceland’s commercial poultry flocks, it is direct and indirect economic costs associated with very likely that waste food from domestic kitchens or H5N1 HPAI in Asia from late 2003 to mid 2005 have bakeries might be used to feed small backyard poultry been estimated to exceed US$ 10 billion (Swayne and flocks. There is a non-negligible likelihood that small Halvorson 2008). Although Iceland does not export backyard poultry flocks will be exposed to HPAI poultry meat, the impact on the domestic industry through consumption of scraps of uncooked poultry would nevertheless be significant. meat.

Infection of wild birds with HPAI usually produces Although wild birds are the reservoirs of all AI no mortality or morbidity (Swayne and Halvorson viruses and play a major role in the introduction of 2008) although recent H5N1 HPAI viruses have been AI viruses in domestic poultry (Swayne and associated with deaths in a number of wild bird Halvorson 2008), surveillance of wildlife during an species in Asia (Ellis et al. 2004; Chen et al. 2005; Sims H5N2 outbreak in poultry in the United States et al. 2005; Webster et al. 2005). The impact on native indicated there was limited transmission of virus from bird species in Iceland cannot be predicted with any domestic poultry to wild birds and that wild birds had degree of confidence. a very limited role in disease dissemination during the outbreak (Hinshaw et al. 1986b; Nettles et al. 1985). However, due to biosecurity measures on commercial

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Sporadic cases of AI infection of humans have been the transmission potential from poultry to humans is documented although these have been rare compared likely to be low (Swayne and Halvorson 2008). to the hundreds of millions of human infections by H1N1 and H3N2 human-adapted influenza viruses The introduction of HPAI would be associated with that occur each year. Human cases typically present non-negligible consequences to the domestic poultry with conjunctivitis, respiratory illness, or flu-like industry, wildlife and human health. symptoms. Recent Asian H5N1 human cases have been closely associated with exposure to infected live or dead poultry in live poultry markets or villages 11.2.4. Risk estimation (Swayne and Halvorson 2008). However, serological surveys of humans in four Thai villages (Dejpichai et Since entry, exposure, and consequence assessments al. 2009) and a Cambodian village (Vong et al. 2006) are non-negligible, the risk estimation is non- found no evidence of neutralising antibodies to negligible and HPAI is assessed to be a risk in H5N1 despite frequent direct contact with poultry unrestricted meat imports from the European Union. likely to be infected with this virus, suggesting that

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Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 12. AVIAN METAPNEUMOVIRUS

12.1. HAZARD IDENTIFICATION 12.1.1. Aetiological agent The clinical diseases associated with aMPV infection of poultry are termed turkey rhinotracheitis (TRT), swollen head syndrome (SHS), and avian Family: Paramyxoviridae, Genus: Metapneumovirus rhinotracheitis (ART). (Gough and Jones 2008). Avian metapneumovirus (aMPV) is classified into subtypes A, B, C, and D on the basis of virus neutralisation and sequence analysis 12.1.2. Iceland status (Bäyon-Auboyer et al. 1999; Cook and Cavanagh 2002). Turkey rhinotracheitis has never been reported in Iceland. Avian rhinotracheitis is listed as a group A Type A and B viruses are found in Europe, Asia, notifiable disease in Act No 25/1993 and sporadic Japan, and South and Central America, whereas type serological surveys since 1998 have returned no C viruses are found in the United States (Seal 1998; positive samples (Willeberg 2013). Ongoing freedom Seal et al. 2000; Turpin et al. 2002). Two atypical is supported by general surveillance (OIE 2013). aMPV isolates recovered in France in 1985 (Bäyon- Auboyer et al. 1999) were later classified as type D 12.1.3. European Union status viruses on the basis of sequence analysis (Bäyon- Auboyer et al. 2000). Table 8 (below) summarises the TRT status of the 28 countries of the European Union based on their official returns to the OIE.

Table 8: Status of turkey rhinotracheitis in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Not reported Croatia Freedom Last occurrence unknown Cyprus Freedom Has never occurred Czech Republic Freedom Last occurrence unknown Denmark Freedom Last reported 2007 Estonia Freedom Has never occurred Finland Freedom Last reported 1999 France Not reported Germany Freedom Last occurrence unknown Greece Freedom Has never occurred Hungary Freedom Last reported June 2010 Ireland Present Clinical disease Italy Freedom Has never occurred Latvia Freedom Has never occurred Lithuania Freedom Last occurrence unknown Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Present Clinical disease Poland Not reported Portugal Freedom Last occurrence unknown Romania Not reported Slovakia Freedom Last occurrence unknown Slovenia Freedom Last occurrence unknown Spain Not reported Sweden Freedom Has never occurred United Kingdom Freedom Last reported December 2011

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 12.1.4. Epidemiology The main sites of virus replication in experimentally infected chickens and poults are the epithelial cells of turbinates and the lung (Majó et al. 1995; Majó et al. Turkeys and chickens are the natural hosts of aMPV 1996). Studies of experimentally-infected 30-week- (Gough and Jones 2008). aMPV infections were old turkeys demonstrated virus localisation in the initially described in South Africa, then Europe, the turbinates and trachea whilst lungs, air sacs, spleen, Middle East, Brazil, and the United States. Apart ovary, liver, kidney, and hypothalamus were all from Australasia, all major poultry rearing regions of negative for virus (Jones et al. 1988). Catelli et al. the world have reported the presence of aMPV (1998) were able to recover large amounts of virus (Gough and Jones 2008). Infection has been from the nasal tissue, sinus tissue, and trachea of estimated to cost the turkey industry in Minnesota experimentally infected chickens and smaller around US$ 15 million annually (Rautenschlein et al. quantities of virus were recovered from the lungs. 2002). No virus was recovered from the kidney, liver, duodenum, bursa of Fabricius, or caecal tonsils. Infected turkeys develop swollen sinuses and nasal Similarly, Pedersen et al. (2001) detected aMPV in the discharge, with hyperaemia and exudation seen in the turbinates, sinus, trachea, and lung of experimentally turbinates, sinuses, and trachea at necropsy, and infected four-week-old poults and found that histopathological changes seen in the turbinates, turbinate tissues were significantly more productive sinuses, and upper and lower trachea (Van de Zande sources of virus and viral RNA than were lung and et al. 1999). tracheal specimens.

Infection of chickens with aMPV presents as a Infection is transmitted to susceptible poultry combination of snicking, conjunctivitis, and swelling through direct contact or, experimentally, using nasal around the eyes, over the head and into the mucus from infected birds inoculated by the submandibular region (Tanaka et al. 1995). Gross intranasal or intratracheal routes (Alexander et al. lesions associated with disease include extensive 1986; McDougall and Cook 1986). There is no yellowish gelatinous to purulent oedema in evidence of vertical transmission (Gough and Jones subcutaneous tissue and congestion of the mucosa of 2008). the head, neck, and wattles (Lu et al. 1994). Following disease introduction, spread of disease aMPV has been associated with mild or subclinical within a country is significantly influenced by the disease in ducks (Toquin et al. 1999; Shin et al. 2000; density of the poultry industry (Jones 1996). Shin et al. 2002) although Pekin ducks have been Contaminated water, live animal movements, shown to be refractory to infection with aMPV when personnel, and equipment have been implicated in inoculated by intranasal instillation (Gough et al. outbreaks although spread of aMPVs has only been 1988). confirmed by direct contact with infected birds (Gough and Jones 2008). Cook (2000) concluded Some surveys found no evidence of aMPV infection that the short persistence time of aMPVs in both in game birds (Gough et al. 1990), but later studies chickens and turkeys and the restricted tissue have demonstrated widespread infection of pheasants distribution of the virus help to minimise the risk of in the United Kingdom (Gough et al. 2001) and Italy transmission through carcases or processed products. (Catelli et al. 2001). There is also serological evidence of aMPV infection in guinea fowl (Litjens et al. 1989) 12.1.5. Hazard identification conclusion and ostriches (Cadman et al. 1994). Using RT-PCR, aMPV was detected in wild Canada geese, blue­ winged teal, sparrows, starlings, a snow goose, and a As there is no evidence for the spread of aMPVs ring-billed gull in the United States (Shin et al. 2000; other than through direct contact with infected birds, Bennett et al. 2002; Bennett et al. 2004). it is unlikely that imported meat or meat products would act as a vehicle to introduce this agent. Avian metapneumovirus is not identified as a hazard in Sequence analysis shows a high sequence identity unrestricted meat imports from the European Union. among wild bird isolates and between wild bird and poultry isolates, suggesting that wild birds may act as a reservoir of infection for poultry (Shin et al. 2000; Bennett et al. 2004).

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Bäyon-Auboyer MH, Jestin V, Toquin D, Gough RE, Cox WJ and Alexander DJ (1990). Cherbonnel M and Eterradossi N (1999). Examination of sera from game birds for antibodies Comparison of F-, G- and N-based RT-PCR against avian viruses. Veterinary Record 127, 110-111. protocols with conventional virological procedures for the detection and typing of turkey rhinotracheitis Gough RE, Drury SE, Aldous E and Laing PW virus. Archives of Virology 144, 1091-1109. (2001). Isolation and identification of an avian pneumovirus from pheasants. Veterinary Record 149, Bäyon-Auboyer MH, Arnauld C, Toquin D and 312. Eterradossi N (2000). Nucleotide sequences of the F, L and G protein genes of two non-A/non-B avian Gough RE and Jones RC (2008). Avian pneumoviruses (APV) reveal a novel APV subgroup. metapneumoviruses. In Diseases of Poultry 12th Journal o f General Virology 81, 2723-2733. Edition, 2008, Ed Saif YM, Blackwell Publishing. Pp. 100-110. Bennet RS, McComb B, Shin HJ, Njenga MK, Nagaraja KV and Halvorson DA (2002). Jones RC, Williams RA, Baxter-Jones C, Savage Detection of avian pneumovirus in wild Canadian CE and W ilding GP (1988). Experimental infection Geese (Branta Canadensis) and blue-winged teal (Anas of laying turkeys with rhinotracheitis virus. discors). Avian Diseases 46, 1025-1029. distribution of virus in the tissues and serological response. Avian Pathology 17, 841-850. Bennett RS, Nezworski J, Velayudhan BT, Nagaraja KV, Zeman DH, Dyer N, Graham T, Jones RC (1996). Avian pneumovirus infection. Lauer DC, Njenga MK and Halvorsen DA questions still unanswered. Avian Pathology 25, 639­ (2004). Evidence of avian pneumovirus spread 648. beyond Minnesota among wild and domestic birds in Central North America. Avian Diseases 48, 902-908. Litjens JB, Kleyn van Willigen FC and Sinke M (1989). A case of swollen head syndrome in a flock Cadman HF, Kelly PJ, Zhou R, Davelaar F and of guinea-fowl. Tijdschrift voor diergeneeskunde 114, Manson PR (1994). A serosurvey using enzyme- 719-720. linked immunosorbant assay for antibodies against poultry pathogens in ostriches (Struthio camelus) from Lu YS, Shien YS, Tsai HJ, Tseng CS, Lee SH Zimbabwe. Avian Diseases 38, 621-625. and Lin DF (1994). Swollen head syndrome in Taiwan — isolation of an avian pneumovirus and Catelli E, Cook JKA, Chesher J, Orbell SJ, Woods serological survey. Avian Pathology 23, 169-174. MA, Baxendale W and Huggins MB (1998). The use of virus isolation, histopathology and Majó N, Allan GM, O’Loan CJ, Pagès A and immunoperoxidase techniques to study the Ramis AJ (1995). A sequential histopathologic and dissemination of a chicken isolate of avian immunocytochemical study of chickens, turkey poults pneumovirus in chickens. Avian Pathology 27, 632­ and broiler breeders experimentally infected with 640. turkey rhinotracheitis virus. Avian Diseases 39, 887­ 896. Catelli E, De Marco MA, Delogu M, Terregino C and Guberti V (2001). Serological evidence of avian Majó N, Martí M, O’Loan CJ, Allan GM, Pagès A pneumovirus infection in reared and free-living and Ramis A (1996). Ultrastructural study of turkey pheasants. Veterinary Record 149, 56-58. rhinotracheitis virus infection in turbinates of experimentally infected chickens. Veterinary Cook JKA (2000). Avian rhinotracheitis. Revue Microbiology 52, 37-48 Scientifique et Technique Office International des Épizooties 19, 602-613. McDougall JS and Cook JKA (1986). Turkey rhinotracheitis: preliminary investigations. Veterinary Cook JKA and Cavanagh D (2002). Detection and Record 118, 206-207 differentiation of avian pneumoviruses (metapneumoviruses). Avian Pathology 31, 117-132.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union OIE (2013). World Animal Health Information Shin HJ, Nagaraja KV, McComb B, Halvorson Database (WAHID) Interface. Available at: DA, Jirjis FF, Shaw DP, Seal BS and Njenga MK http: / /www.oie.int/wahis 2/public/wahid.php/Wah (2002). Isolation of avian pneumovirus from mallard idhome/Home, last accessed 1 July 2103. ducks that is genetically similar to viruses isolated from neighbouring commercial turkeys. Virus Pedersen JC, Senne DA, Panigrahy B and Research 83, 207-212. Reynolds DL (2001). Detection of avian pneumovirus in tissues and swab specimens from Tanaka M, Takuma H, Kokumai N, Oishi E, infected turkeys. Avian Diseases 45, 581-592. Obi T, Hiramatsu K and Shimizu Y (1995). Turkey rhinotracheitis virus isolated form broiler Rautenschlein S, Sheikh AM, Patnayak DP, chickens with swollen head syndrome in Japan. Miller RL, Sharma JM and Goyal SM (2002). Journal of Veterinary Medical Science 57, 939-941. Effect of an immunomodulator on the efficacy of an attenuated vaccine against avian pneumovirus in Toquin D, Bäyon-Auboyer MH, Eterradossi N, turkeys. Avian Diseases 46, 555-561. Jestin V and Morin H (1999). Isolation of a pneumovirus from a Muscovy duck. Veterinary Record Seal BS (1998). Matrix protein gene nucleotide and 145, 680. predicted amino acid sequence demonstrate that the first US avian pneumovirus isolate is distinct from Turpin EA, Perkins LEL and Swayne DE (2002). European strains. Virus Research 58, 45-52. Experimental infection of turkeys with avian pneumovirus and either Newcastle disease virus or Seal BS, Sellers HS and Meinersmann RJ (2000). Escherichia coli. Avian Diseases 46, 412-422. Fusion protein predicted amino acid sequence of the first US avian pneumovirus isolate and lack of Van de Zande S, Nauwynck H, De Jonghe S and heterogeneity among other US isolates. Virus Research Pensaert M (1999). Comparative pathogenesis of a 66, 139-147. subtype A with a subtype B avian pneumovirus in turkeys. Avian Pathology 28, 239-244. Shin HJ, Njenga MK, McComb B, Halvorson DA and N agaraja KV (2000). Avian pneumovirus W illeberg P (2013). Chapter 5. Notification and (APV) RNA from wild and sentinel birds in the US animal disease surveillance. In: Risk assessments has genetic homology with APV isolates from regarding open trade in live animals to Iceland. Icelandic domestic turkeys. Journal of Clinical Microbiology 38, Food and Veterinary Authority (MAST), Reykjavik, 4282-4284 Iceland. Pp 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 13. AVIAN PARAMYXOVIRUSES (EXCEPT NEWCASTLE DISEASE VIRUS)

13.1. HAZARD IDENTIFICATION 13.1.1. Aetiological agent

Family: Paramyxoviridae, Subfamily: Paramyxovirinae, Genus: Avulavirus (Alexander and Senne 2008). Nine serogroups of avian paramyxoviruses are recognised, APMV-1 to APMV-9. APMV-1 is assessed in Chapter 24 of this document. The prototype strains of APMV-2 to APMV-9 were summarised by Alexander and Senne (2008) as shown in Table 9 (below):

Table 9. Prototype viruses, host range of avian paramyxoviruses (from Alexander and Senne 2008).

Prototype virus strain Usual natural Other hosts Disease produced in poultry hosts

APMV2/chicken/California/Yucaipa/56 Turkeys, Chickens, Mild respiratory disease or egg passerines psittacines, rails production problems, severe if exacerbation occurs

APMV3*/turkey/Wisconsin/68 Turkeys None Mild respiratory disease but severe egg production problems worsened by exacerbating organisms or environment

APMV3*/parakeet/Netherlands/449/75 Psittacines, None known None known passerines

APMV4/duck/Hong Kong/D3/75 Ducks Geese None known

APMV 5/budgerigar/Japan/ Kunitachi/74 Budgerigars None known No infections of poultry reported

APMV6/duck/Hong Kong/199/77 Ducks Geese, rails, Mild respiratory disease and turkeys slightly elevated mortality in turkeys; none in ducks or geese

APMV7/dove/Tennessee/4/75 Pigeons, doves Turkeys, Mild respiratory disease in ostriches turkeys

APMV8/goose/Delaware/1053/76 Ducks, geese None known No infection of poultry reported

APMV9/domestic duck/New Ducks None known Inapparent infection of York/22/78 commercial ducks.

*Serological tests may distinguish between turkey and psittacine isolates.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 13.1.2. Iceland status APMV-3 has been isolated from turkey flocks (Tumova et al. 1979; Alexander 1980; Alexander et al. 1983; MacPherson et al. 1983) although APMV-3 Avian paramyxoviruses have not been recorded in isolates are mainly associated with captive psittacine Iceland. For the purposes of this assessment Iceland and passerine birds (Shortridge et al. 1991). is assumed to be free from these viruses. Experimental infection of 1-day-old chicks with APMV-3 resulted in severe growth impairment 13.1.3. European Union status whereas no clinical signs followed experimental infection of 6-week-old birds (Alexander and Collins With the possible exception of APMV-5, all avian 1982). Natural infection of turkey flocks with paramyxovirus serogroups have been recognised in APMV-3 has been associated with reduced egg the European Union (see below). production in breeder farms (Alexander et al. 1983; MacPherson et al. 1983) and mild respiratory disease (Tumova et al. 1979). 13.1.4. Epidemiology

APMV-4 has been recovered from ducks in the APMV-2 and APMV-4 tend to be associated with United States and Hong Kong (Alexander et al. 1979) domestic chickens, whilst APMV-4, APMV-6, and as well as from wild ducks in Japan (Nerome et al. APMV-9 are recognised in domestic ducks 1984). (Alexander 1993). Infection with APMV-2, APMV- 3, APMV-6, and APMV-7 has been associated with turkeys (Bankowski et aL 1968; Alexander 1980; Saif et APMV-5 was isolated from budgerigar flocks in al. 1997; Alexander 2000). Other avian Tokyo in 1974 (Nerome et al. 1978). paramyxoviruses recovered from poultry are usually identified as incidental findings during surveillance APMV-6 has been isolated from turkeys with reduced for avian influenza (Shortridge et aL 1980; Alexander egg production and mild respiratory problems and Senne 2008). (Alexander 2000). APMV-6 isolates have also been recovered from migrating wild ducks in Japan A wider range of APMV serotypes have been (Nerome et al. 1984), as well as from ducks and demonstrated in wildfowl, with a serological survey in chickens in Hong Kong (Shortridge et al. 1980). Spain of aquatic wildfowl identifying exposure to APMV-1, APMV-2, APMV-3, APMV-4, APMV-6, APMV-7 has been isolated from an outbreak of APMV-7, APMV-8, and APMV-9 (Maldonado et al. respiratory disease in a turkey breeder flock in the 1995). United States. Experimental inoculation of specific- pathogen-free poults with this isolate resulted in APMV-2 was first described in 1960 (Bankowski et al. rhinitis and airsaccultitis (Saif et al. 1997). 1960; Dinter et al. 1964), and a subsequent survey of turkey flocks indicated that APMV-2 was widespread As already noted, other avian paramyxoviruses of in the United States (Bankowski et al. 1968). APMV- poultry are usually identified as incidental findings 2 has also been recovered from both chickens and during surveillance for avian influenza (Shortridge et ducks (Lipkind et aL 1982; Goodman and Hanson al. 1980; Alexander and Senne 2008). 1988; Shihmanter et al. 1997). APMV-2 viruses have also been reported in Canada, the former Soviet APMV-2 and APMV-3 infection leads to shedding Union, Japan, the United Kingdom, Germany, from the respiratory and intestinal tracts of poultry Senegal, Czech Republic, Italy, and Israel. The (Alexander and Senne 2008). However, there is presence of APMV-2 in Israel and Italy has been limited information concerning the epidemiology of associated with the importation of turkey products avian paramyxoviruses other than APMV-1 from North America although subclinical infection of (Alexander 2000). Given the similarities between migratory passeriformes has also been suggested as a APMV-1 and other avian paramyxoviruses in means of international spread (Alexander 1980). infection and replication, it has been suggested that Widespread seropositivity to APMV-2 has been the same mechanisms of introduction and spread described in broilers in China (Zhang et aL 2006; would apply (Alexander 2000). Zhang et al. 2007). 13.1.5. Hazard identification conclusion APMV-2 infection of turkeys may be subclinical or cause mild respiratory signs (Bankowski et al. 1968; APMV-2 and APMV-6 have been associated with Bradshaw and Jensen 1979), although more severe chickens, whereas APMV-2, APMV-4, and APMV-6 respiratory disease may be seen when there are co­ have been associated with domestic ducks, and infections with other pathogens (Lang et al. 1975). APMV-2, APMV-3, APMV-6, and APMV-7 have Experimental infection of turkey hens with APMV-2 been associated with turkeys. was shown to have a profound effect on egg hatchability and poult yield (Bankowski et al. 1981).

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Replication of avian paramyxoviruses (except any data to support this, it is assumed that some of Newcastle disease) is assumed to be limited to the this may be discarded as raw tissue prior to cooking intestinal and respiratory tracts. Although respiratory and therefore become accessible to poultry being fed and intestinal tissues will be removed from chicken, domestic food waste. There is therefore assessed to duck, and turkey carcases, remnants of these tissues be a non-negligible likelihood of backyard poultry may remain following processing. APMV-2, APMV- exposure from raw scraps generated during the 3, APMV-4, APMV-6, and APMV-7 are therefore domestic preparation of imported whole poultry identified as potential hazards in imported whole carcases. poultry carcases. There have been no reports describing the spread of 13.2. RISK ASSESSMENT avian paramyxoviruses (other than Newcastle disease 13.2.1. Entry assessment virus) from backyard flocks to commercial poultry. Commercial poultry farms in Iceland are unlikely to feed waste food and there are no commercial free­ Infection with APMV-2, APMV-3, APMV-6, or range poultry flocks in Iceland. Commercial poultry APMV-7 may be associated with mild respiratory flocks in Iceland have a high standard of biosecurity signs so infected flocks may not be detected during and there is a negligible likelihood of significant routine ante-mortem and post-mortem inspection. contact between commercial flocks and backyard Infected tissues would be limited to any remnants of flocks. The likelihood of commercial poultry flocks respiratory or intestinal tissues remaining in poultry being exposed to avian paramyxoviruses associated carcases after processing. The likelihood of entry is with imported poultry meat is assessed to be therefore assessed to be very low. negligible.

13.2.2. Exposure assessment 13.2.3. Consequence assessment

There are a small number of large commercial poultry APMV-2, APMV-3, APMV-6, and APMV-7 flocks in Iceland and currently no commercial free­ infections of poultry have been associated with mild range poultry farms. Backyard poultry keeping in respiratory signs. However, as discussed above, these Iceland is becoming increasingly popular and official consequences would be limited to small, non­ data indicates over 403 poultry flocks in Iceland with commercial, backyard flocks. Although NDV is <100 hens. Although waste food would not be used recognised to infect humans, there have been no as feed in Iceland’s commercial poultry flocks, it is reports of other APMV serotypes infecting humans very likely that waste food from domestic kitchens or (Alexander and Senne 2008) so there would be bakeries might be used to feed small backyard poultry negligible consequences for human health. flocks. The heat sensitivity of avian paramyxoviruses is likely to be similar to that of APMV-1. Assuming The consequences of introduction are therefore that the mechanisms of introduction and spread for APMV-1 are the same for other avian assessed to be negligible. paramyxoviruses (Alexander 2000), there is assessed to be a negligible likelihood of backyard poultry being 13.2.4. Risk estimation exposed to APMV-2 from scraps of cooked poultry meat. As the consequence assessment is negligible, the risk estimate is negligible and avian paramyxoviruses Any respiratory or intestinal tissue remnants in (excluding Newcastle disease virus) are not assessed imported poultry carcases would be unlikely to be to be a risk in unrestricted meat imports from the removed prior to cooking although, in the absence of European Union.

References

Alexander DJ (1980). Avian paramyxoviruses. Alexander DJ, Aymard M, Kessler N and Collins Veterinary Bulletin 50, 737-752. MS (1979). Antigenic and structural relationships between avian paramyxoviruses isolated form ducks Alexander DJ (1993). Paramyxovirus infection. In in Hong Kong and Mississippi, U.S.A. Journal o f Virus Infections of Birds (Eds McFerran JB and General Virology 44, 839-842. McNulty MS) Elsevier Science Publishers. Pp. 321­ 340. Alexander DJ and Collins MS (1982). Pathogenicity of PMV- Alexander DJ (2000). Newcastle disease and other 3/parakeet/Netherlands/449/75 for chickens. Avian avian paramyxoviruses. Revue Scientifique et Technique Pathology 11, 179-185. Office International des Épizooties 19, 443-462.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Alexander DJ, Pattisson M and Macpherson I Maldonado A, Arenas A, Tarradas MC, (1983). Avian paramyxoviruses of PMV-3 serotype Luque I, Astorga R, Perea JA and Miranda in British turkeys. Avian Pathology 12, 469-482. A (1995). Serological survey for avian paramyxoviruses from wildfowl in aquatic Alexander DJ and Senne DA (2008). Newcastle habitats in Andalusia. Journal of Wildlife Diseases disease, other avian paramyxoviruses, and 31, 66-69. pneumovirus infections. In Diseases o f Poultry 12th Edition. Ed Saif YM, Blackwell Publishing. Pp. 75­ Nerome K, Nakayama M, Ishida M, Fukumi H 115. and Morita A (1978). Isolation of a new avian paramyxovirus from budgerigar (Melopsittacus Bankowski RA, Corstvet RE and Clark GT undulatus). Journal of General Virology 38, 293-301. (1960). Isolation of an unidentified agent from the respiratory tract of chickens. Science 132, 292-293. Nerome K, Shibata M, Kobayshi S, Yamaguchi B, Yoshioka Y, Ishida M and Oya A (1984). Bankowski RA, Conrad RD and Reynolds B Immunological and genomic analyses of two (1968). Avian influenza and paramyxoviruses serotypes of avian paramyxovirus isolated from wild complicating respiratory disease diagnosis in poultry. ducks in Japan. Journal of Virology 50, 649-653 Avian Diseases 12, 259-278. Saif YM, Mohan R, Ward L, Senne DA, Bankowski RA, Almquist J and Dombrucki J Panigrahy B and Dearth RN (1997). Natural and (1981). Effect of paramyxovirus Yucaipa on fertility, experimental infection of turkeys with avian hatchability and poult yield of turkeys. Avian Diseases paramyxovirus-7. Avian Diseases 41, 326-329. 25, 517-520. Shihmanter E, Weisman Y, Manwell R, Bradshaw GL and Jensen MM (1979). The Alexander D and Lipkind M (1997). Mixed epidemiology of Yucaipa virus in relationship to the paramyxovirus infection of wild and domestic birds acute respiratory disease syndrome in turkeys. Avian in Israel. Veterinary Microbiology 58, 73-78. Diseases 23, 539-542. Shortridge KF, Alexander DJ and Collins MS Dinter Z, Hermodsson S and Hermodsson L (1980). Isolation and properties of viruses from (1964). Studies on myxovirus Yucaipa: Its poultry in Hong Kong which represent a new (sixth) classification as a member of the paramyxovirus distinct group of avian paramyxoviruses. Journal o f group. Virology 22, 297-304. General Virology 49, 255-262.

Goodman BB and Hanson RP (1988). Isolation of Shortridge KF, Burrows D and Erdei J (1991). avian paramyxovirus-2 from domestic and wild birds Potential danger of avian paramyxovirus type 3 to in Costa Rica. Avian Diseases 32, 713-717. ornithological collections. Veterinary Record 129, 363­ 364. Lang G, Gagnon A and Howell J (1975). Occurrence of paramyxovirus Yucaipa in Canadian Tumova B, Robinson JH and Easterday BC poultry. Canadian Veterinary Journal 16, 233-237. (1979). A hitherto unreported paramyxovirus of turkeys. Research in Veterinary Science 27, 135-140. Lipkind MA, Weisman Y, Shihmanter E, Shoham D and Aronovici A (1982). Isolation of Zhang GZ, Zhao JX, Wang HW, Yang AM, Yucaipa-like avian parmyxovirus from a wild mallard Bu CY and Wang M (2006). Isolation, duck (Anas platyrhynchos) wintering in Israel. Veterinary identification, and comparison of four isolates Record 110, 15-16. of avian paramyxovirus serotype 2 in China. Avian Diseases 50, 386-390. MacPherson I, Watt RG and Alexander DJ (1983). Isolation of avian paramyxovirus, other than Zhang GZ, Zhao JX and Wang M (2007). Newcastle disease virus, from commercial poultry in Serological survey on prevalence of antibodies Great Britain. Veterinary Record 112, 479-480. to avian paramyxovirus serotype 2 in China. Avian Diseases 51, 137-139.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 14. BORDER DISEASE VIRUS

14.1. HAZARD IDENTIFICATION 14.1.1. Aetiological agent The most serious consequences of BDV infection occur when the virus infects ewes during pregnancy. In the absence of clinical signs BDV spreads rapidly Border disease is a congenital disease of sheep first to the placenta and crosses to the foetus. The reported from the Border region between England immune response of the ewe quickly eliminates all and Wales (Hughes et aL 1959). Border disease virus virus from the maternal tissues but it has no effect in (BDV) is a Pestivirus in the family Flaviviridae and is the foetus where virus can persist. The outcome of closely related to classical swine fever virus and bovine viral the foetal infection depends on the strain and dose of diarrhoea virus (Nettleton and Willoughby 2008). virus, the breed of the foetus, and its ability to repair damage but most important is the stage of foetal 14.1.2. Iceland status development at which infection occurs (Nettleton 1990). Border disease has never been reported in Iceland. The most dangerous time for a foetus to become 14.1.3. European Union status infected is in the first 60 days when BDV replication will be uncontrolled, resulting in foetal death. In lambs that survive infection in early gestation, virus is Border disease has been described throughout the widespread in virtually all organs. The principal world. There have been reports of this disease from pathological findings are myelin deficiency in the much of Europe including Scotland, Ireland, Greece, central nervous system which accounts for the tremor the Netherlands, Germany, France, and Sweden and an increase in the number of primary hair (Barlow and Dickinson 1965; Hamilton and Donnelly follicles causing 'hairiness'. Such lambs are tolerant to 1970; Spais et al. 1975; Terpstra 1977; Nettleton the virus and have a persistent infection usually for 1990). life (Terpstra 1981). Infections later in gestation can result in widespread inflammatory lesions in the 14.1.4. Epidemiology central nervous system leading to cerebral cavitation and cerebellar dysplasia (Barlow 1983). These Almost all field isolates of BDV are non-cytopathic in individuals frequently have severe nervous signs and cell cultures, although cytopathic strains have been major locomotor disturbances and have a high described (Vantsis et a l 1976; Laude and Gelfi 1979). concentration of serum antibody to BDV (Roeder et While the non-cytopathic biotypes cause congenital al 1987). disease and persistent infection, cytopathic isolates have been recovered from sheep dying of a 'mucosal Foetal infection after 80 days gestation is met by an disease-like' syndrome (Barlow et al. 1983; Gardiner et immune system capable of eliminating the virus. al. 1983). Foetal death is rare and virtually all lambs will be born apparently normal. They will be free of virus A variety of clinical signs are associated with the but have demonstrable antibody (Nettleton 1990). presence of BDV in a flock. An excessive number of abortions and barren ewes and the birth of small Persistent infections with BDV can be established weak lambs has been associated with BDV. Lambs only if lambs are infected during their first 80 days of may be born with abnormal body conformation, gestation. Virus persists in most tissues and the tremor and/or fleece changes sometimes with lambs remain a potent source of infection. Within abnormal pigmentation (hairy-shaker' or 'fuzzy groups of persistently infected lambs some animals lambs'). Ill-thrift may be seen in older lambs can suffer from chronic wasting, others can develop (Nettleton 1990). excessive ocular and nasal discharges sometimes with respiratory distress, while others develop an Infection of normal healthy sheep with virtually all intractable scour and die within 4 weeks. Cytopathic BDV isolates is short-lived and mostly sub-clinical. BDV can be recovered from the gut of these lambs Mild pyrexia and transient lymphopaenia coincide and this syndrome has several similarities with bovine with viraemia, but with the production of neutralising mucosal disease (Barlow et al. 1983; Gardiner et al. antibodies 2 to 3 weeks after infection these signs 1983). disappear (Nettleton 1990). Sheep-to-sheep contact is the principal way in which BDV is spread, and the most potent source of virus is the persistent excretor. Bought-in PI sheep have been shown to introduce BDV into a susceptible flock and cause a serious outbreak of border disease,

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union and many other outbreaks of border disease have a history of introduction of new stock at the beginning of the breeding season (Vantsis et aL 1979; Bonniwell et aL 1987). Transmission though meat and meat products has not been reported.

14.1.5. Hazard identification conclusion

There is no evidence to suggest that BDV is likely to be transmitted through the international trade in meat. BDV is not identified as a hazard in unrestricted meat imports from the European Union.

References

Barlow RM (1983). Some interactions of virus and Nettleton PF (1990). Pestivirus infections in maternal/foetal immune mechanisms in border ruminants other than cattle. Revue Scientifique et disease of sheep. Progress in Brain Research 59, 255-268. Technique Office International des Épiyooties 9, 131-150.

Barlow RM and Dickinson AG (1965). On the Nettleton PF and Willoughby K (2008). Chapter pathology and histochemistry of the central nervous 2.7.1. Border disease. In: OIE Manual of Diagnostic system in border disease of sheep. Research in Tests and Vaccines for Terrestrial Animals, OIE, Veterinary Science 6, 230-237. Paris. Available at: http: //www.oie.int/fileadmin/Home/eng/Health st Barlow RM, Gardiner AC and Nettleton PF andards/tahm/2.07.01 BORDER DIS.pdf, last (1983). The pathology of a spontaneous and accessed 22 September 2013. experimental mucosal disease-like syndrome in sheep recovered from clinical border disease. Journal o f Roeder PL, Jeffrey M and Drew TW (1987). Comparative Pathology 93, 451-461. Variable nature of border disease on a single farm: the infection status of affected sheep. Research in Bonniwell MA, Nettleton PF, Gardiner AC, Veterinary Science 43, 28-33. Barlow RM and Gilmour JS (1987). Border disease without nervous signs or fleece changes. Veterinary Spais AG, Papadopouloso O and Vantsis JT Record 120, 246-249 (1975). An extensive outbreak of border disease in Greece. Proceedings of the 20th World Veterinary Gardiner AC, Nettleton PF and Barlow RM Congress, Salonika, 622. (1983). Virology and immunology of a spontaneous and experimental mucosal disease-like syndrome in Terpstra C (1977). Diagnosis of border disease by sheep recovered from clinical border disease. Journal direct immunofluorescence. Veterinary Science of Comparative Pathology 93, 463-469. Communications 1, 75-77.

Hamilton AF and Donnelly JC (1970). A new Terpstra C (1981). Border disease. Virus persistence, condition in lambs in Ireland. Veterinary Record 86, antibody response and transmission studies. Research 581. in Veterinary Science 30, 185-191.

Hughes LE, Kershaw GF and Shaw IG (1959). 'B' Vantsis JT, Barlow RM, Fraser J, Rennie JC and or border disease. An undescribed disease of sheep. Mould DL (1976). Experiments in border disease Veterinary Record 71, 313-317. VIII. Propagation and properties of a cytopathic virus. Journal of Comparative Pathology 86, 111-120. Laude H and Gelfi J (1979). Properties of border disease virus as studied in a sheep cell line. Archives o f Vantsis JT, Linklater KA, Rennie JC and Barlow Virology 62, 341-346. RM (1979). Experimental challenge and infection of ewes following a field outbreak of border disease. Journal of Comparative Pathology 89, 331-339.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 15. BOVINE VIRAL DIARRHOEA VIRUS

15.1. HAZARD IDENTIFICATION 15.1.1. Aetiological agent 15.1.2. Iceland status

Family: Flaviviridae; genus: Pestivirus, species: Bovine Bovine viral diarrhoea (BVD) has never been viral diarrhoea virus (BVDV) (Simmonds et al. 2012). reported in Iceland and is listed as a group B There are two genotypes, BVDV1 and BVDV2 notifiable disease in Act No 25/1993. In 1992 and (Booth et al. 1995). In each genotype both cytopathic 1994 serological surveys for BVD were conducted and noncytopathic isolates occur. and systematic surveillance has been carried out since 2007 (Willeberg 2013). There is general and targeted The BVDV genome may undergo mutation events surveillance for this disease (OIE 2013). commonly during replication. Therefore, genomic recombination can occur in noncytopathic viruses 15.1.3. European Union status from either genotype resulting in cytopathic viruses. In recent years, there been speculation that BVDV2 isolates cause a greater severity of disease with higher Table 10 (below) summarises the BVD status of the viral titres than isolates within the genotype BVDV1 28 countries of the European Union based on their (Potgieter 2004; Radostits et al. 2007). official returns to the OIE.

Table 10: Status of bovine viral diarrhoea in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other A ustria Present Clinical disease Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 2010 Croatia Freedom Last occurrence unknown Cyprus Present Clinical disease Czech Republic Freedom Last reported June 2011 Denmark Present Clinical disease E stonia Present No clinical disease Finland Freedom Last reported June 201 France Present Clinical disease Germany Present Clinical disease Greece Freedom Last occurrence unknown Hungary Present Restricted to certain zones Ireland Present Clinical disease Italy Freedom Last reported June 2012 Latvia Present No clinical disease L ithuania Present No clinical disease Luxembourg Present Clinical disease Malta Freedom Last reported 2004 Netherlands Present Clinical disease Poland Not reported Portugal Present Clinical disease Romania Not reported Slovakia Freedom Last reported 2006 Slovenia Present Clinical disease Spain Present Disease limited to one or more zones Sweden Freedom Last reported December 2011 United Kingdom Present Clinical disease

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 15.1.4. Epidemiology as a source of infection for cattle is unknown (Radostits et al. 2007). Radostits et al. (2007) do not identify meat as a possible method for transmitting BVD is primarily a disease of cattle although infection to ruminants or pigs. antibodies to BVDV have been described in a variety of other ruminants and pigs (Horner 2000; Le Potier et aL 2006; Radostits et aL 2007). However, infection However, Bratcher et al. (2012) have shown that of small ruminants and pigs is not associated with BVDV may be present in skeletal muscle derived clinical disease (Le Potier et aL 2006). from persistently infected cattle, and readily survives aging for 21 days at 4°C, freezing, thawing, and cooking to temperatures of less than or equal to BVDV1 infection of non-pregnant cattle usually 70°C. results in a mild disease with pyrexia and leukopenia from about 3-7 days accompanied by viraemia and nasal excretion of virus (Brownlie 2005). Clinical 15.1.5. Hazard identification conclusion signs are occasionally accompanied by diarrhoea (Potgieter 2004). Cattle are usually infected before Although there is little historical evidence to suggest they become pregnant, resulting in an immune BVDV is likely to be transmitted through the population. However, infection of naïve pregnant international trade in meat, recent studies have shown animals, particularly during the first trimester, may virus may be present in meat derived from result in death of the conceptus or full term, or near persistently infected cattle and persist during storage. full term, delivery of immunotolerant persistently Iceland is free from BVD whereas infection has been infected calves. described in many countries of the European Union. BVDV is identified as a potential hazard in bovine BVDV2 strains associated with a more severe form meat and meat products imported from the of the disease characterised by up to 10% mortality European Union. accompanied by severe leucopenia and haemorrhagic disease were first described in the United States 15.2. RISK ASSESSMENT (Pellerin et al. 1994; Brownlie 2005; Potgieter 2005). 15.2.1. Entry assessment

Persistently infected immunotolerant cattle may be clinically normal or show signs of ill-thrift and die Cattle are the primary host for BVDV. However, a within a year. These individuals are infected with number of other ruminants and pigs have been noncytopathic strains of the virus (Brownlie 2005) shown to be susceptible to infection. then acquire an infection of a cytopathic BVDV strain, which leads to the development of mucosal Animals either acutely or persistently infected with disease. The secondary cytopathic strain may arise BVDV could be viraemic at slaughter. The virus may from a mutation of the persistent noncytopathic be found throughout the body of persistently infected strain or from infection with a new extrinsic animals. Ante-mortem and post-mortem inspection cytopathic virus (Potgieter 2004; Brownlie 2005). may not detect these infected animals since disease is Mucosal disease is invariably fatal. In acute cases mostly mild or subclinical. No lesions were seen in death occurs within 2-21 days while in chronic cases those carcasses studied by Bratcher et al. (2012) the animal may survive for up to 18 months derived from persistently infected cattle. (Potgieter 2004). BVDV in whole and ground meat (skeletal muscle) is Although natural infection in pigs usually causes no consistently inactivated when cooked to temperatures clinical signs, experimental infection of naïve greater than or equal to 75°C (Bratcher et al. 2012). pregnant sows caused infection of foetuses, which Consequently, imported meat that has not been resulted in foetal mortality, or birth of persistently cooked to at least 75°C could harbour BVDV. infected immunotolerant piglets. Piglets that have been infected in utero may excrete large quantities of Therefore, for fresh meat from cattle originating virus, but when infected at birth they excrete little or from countries where BVDV occurs, the likelihood no virus and do not spread infection to in-contact for entry is assessed to be non-negligible. animals. Some BVDV strains experimentally inoculated into piglets caused no clinical disease 15.2.2. Exposure assessment although virus could be recovered from blood and tissues (Le Potier et aL 2006). For livestock to become infected they would have to be exposed to contaminated meat. Since herbivorous BVDV is primarily transmitted by direct contact with animals do not naturally eat meat, the likelihood of persistently infected viraemic cattle or transplacentally exposure by this pathway is so low that it is to the foetus. Pigs and susceptible small ruminants considered to be negligible. The only other potential could be infected when in close contact with infected route of exposure for livestock is feeding meat to cattle. The importance of pigs and small ruminants pigs.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union As a result of their recent study, Bratcher et aL (2012) transmitting infection to any other animal species, advised that care should be taken to ensure they are likely to be dead-end hosts. susceptible hosts such as pigs are not fed improperly cooked meat, or waste food originating from cattle The likelihood of exposure is therefore assessed to be persistently infected with BVDV. very low.

Although there are a small number of commercial pig 15.2.3. Consequence assessment farms in Iceland, there has been an increase in the number of people keeping a small number of pigs as a ‘hobby’. In addition there has been an increase in The occurrence of disease would be dependent on the number of sheep or cattle farms that keep a small the pathogenicity of the introduced viral strain and herd of pigs. Although it is unlikely that commercial whether pregnant sows were exposed (Potgieter pig farms in Iceland would use kitchen waste as a 2004). BVDV is primarily a disease of cattle. source of feed, it is highly likely that kitchen waste Although experimentally inoculating pigs may would be used as an inexpensive source of feed for sometimes cause disease, natural BVDV infections of pigs in small hobby herds. pigs rarely cause disease (Le Potier et aL 2006). There are no reports of naturally infected pigs transmitting infection to any other animal species. Experimentally, BVDV inoculation of naïve pregnant sows has resulted in persistently infected immunotolerant piglets. Some persistently infected As the virus does not infect humans, there would be piglets shed virus and were able to transmit infection no consequences for human health. by direct contact to other piglets. However, piglets experimentally infected at birth excreted little or no Reflecting the above, the consequences of virus and did not spread infection (Le Potier et aL introducing BVDV through the importation of fresh 2006). Moreover, some BVDV strains experimentally meat from the European Union are assessed to be inoculated into piglets caused no clinical disease (Le negligible. Potier et al. 2006). 15.2.4. Risk estimation In naturally occurring infection of pigs with BVDV, disease is rare. As a source of infection, pigs are not As the consequence assessment is negligible, the risk epidemiologically important when compared to estimate is negligible and BVDV is not assessed to be persistently infected cattle. Since disease in pigs is a risk in unrestricted meat imports from the rare and there are no reports of naturally infected pigs European Union.

References

Booth PJ, Stevens DA, Collins ME and Brownlie Le Potier M-F, Mesplede A and Vannier P J (1995). Detection of bovine viral diarrhoea virus (2006). Classical swine fever and other pestiviruses. antigen and RNA in oviduct and granulosa cells of In: Straw BE, Zimmerman JJ, D'Allaire S, Taylor D persistently infected cattle. Journal of Reproduction and (eds.) Diseases o f Swine. Blackwell Publishing, Oxford, Fertility 105, 17-24. U K Pp. 309-322.

Bratcher CL, Wilborn BS, Finegan HM, Rodning OIE (2013). World Animal Health Information SP, Galik PK, Riddell KP, Marley MS, Zhang Y, Database (WAHID) Interface. Available at: Bell LN and Givens MD (2012). Inactivation at http://www.oie.int/wahis 2/public/wahid.php/Wah various temperatures of bovine viral diarrhea virus in idhome/Home, last accessed 1 July 2103. beef derived from persitently infected cattle. Journal o f Animal Science 90, 635-641. Pellerin C, van den Hurk J, Lecomte J and Tussen P (1994). Identification of a new group of Brownlie J (2005). Bovine virus diarrhoea virus - bovine viral diarrhea virus strains associated with Strategic directions for diagnosis and control, BVDV severe outbreaks and high mortalities. Virology 203, Symposium 2005. VetLearn, Massey University, 260-268. Palmerston North, Wellington, New Zealand. Pp. 1­ 19. Potgieter LND (2004). Bovine viral diarrhoea and mucosal disease. In: Coetzer JAW , Tustin RC (eds.) Horner GW (2000). Typing of New Zealand strains Infectious Diseases of Livestock. Oxford University Press, of pestivirus. Surveillance 27 (3), 16. Cape Town. Pp. 946-969.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Radostits OM, Gay, CC, Hinchcliff KW and W illeberg P (2013). Chapter 5. Notification and Constable PD (2007). Bovine viral diarrhea, animal disease surveillance. In: Risk assessments mucosal disease. Bovine pestivirus disease complex. regarding open trade in live animals to Iceland. Icelandic In: Veterinary Medicine A textbook o f the diseases of cattle, Food and Veterinary Authority (MAST), Reykjavik, horses, sheep, pigs, and goats. Saunders Elsevier, Iceland. Pp. 59-90. Edinburgh. Pp. 1248-1277.

Simmonds P, Becher P, Collett MS, Gould EA, Heinz FX, Meyers G, Monath T, Pletnev A, Rice CM, Stiasny K, Theil HJ, Weiner A and Bukh J (2012). Genus Pestivirus. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds.) Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Amsterdam. Pp. 1010-1014.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 16. CAPRIPOXVIRUS

16.1. HAZARD IDENTIFICATION 16.1.1. Aetiological agent 16.1.2. Iceland status

Sheep pox and goat pox are acute or subacute Sheep pox and goat pox have never been reported in contagious and often fatal diseases of sheep and Iceland and is listed as a group A notifiable disease in goats, caused by a virus belonging to the genus Act No 25/1993 (Willeberg 2013). Ongoing freedom Capripoxvirus in the family Poxviridae (Fauquet et al. is supported by general surveillance (OIE 2013). 2005). Most strains of the virus are specific to the host species from which they are isolated, but in some countries strains exist that can infect both 16.1.3. European Union status sheep and goats (Kitching 2004). Table 11 (below) summarises the sheep and goat pox status of the 28 countries of the European Union based on their official returns to the OIE.

Table 11: Status of sheep and goat pox in European Union countries based on their official return to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported 1954 Belgium Freedom Has never occurred Bulgaria Freedom Last reported September 199611 Croatia Freedom Last reported 1955 Cyprus Freedom Last reported July 1989 Czech Republic Freedom Last reported 1950 Denmark Freedom Last reported 1879 Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Last reported 1964 Germany Freedom Last reported 1920 Greece Freedom Last reported 2007 Hungary Freedom Last reported 1957 Ireland Freedom Last reported 1850 Italy Freedom Last reported May 1983 Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Last occurrence unknown Malta Freedom Has never occurred Netherlands Freedom Last reported 1893 Poland Freedom Last reported 1950 Portugal Freedom Last reported 1970 Romania Freedom Last reported 1957 Slovakia Freedom Last reported 1950 Slovenia Freedom Has never occurred Spain Freedom Last reported 1968 Sweden Freedom Last reported 1934 United Kingdom Freedom Last reported 1866

11 At the time of writing, an outbreak of sheep and goat pox was reported in Bulgaria on 23 September 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 16.1.4. Epidemiology Viraemia starts 3 days after infection and lasts 10-12 days. Peak virus titres in skin nodules persist from day 7 to day 14, after which they decline as serum The clinical signs of capripox virus infection vary antibodies develop (Merza and Mushi 1990). considerably with the strain of the virus and the Nodules usually scab and persist for several weeks, species and breed of host (Kitching and Carn 2004). healing to form a permanent, depressed scar. Lesions The morbidity rate in sheep may be as high as 70%; within the mouth ulcerate and constitute an mortality varies from 5 to 50% in adult animals and it important source of virus for infection of other may be even higher in lambs. Both morbidity and animals (Fenner 1996). mortality rates are generally lower in goats. Mild and inapparent infections can also occur (Kitching 2004). Recovery and healing of skin lesions may take 5-6 weeks (Merza and Mushi 1990). High concentrations The effects of disease are seen in the skin and in the of virus occur in lesion material. As with other pox lungs. Infected animals shed virus in all excretions viruses, infectivity is destroyed by exposure to direct and secretions (Kitching 2004). Transmission may be sunlight, but it is retained in dark stables for long through inhalation of virus in contaminated water periods, particularly in scabs shed by infected droplets, dust or dry skin scabs, or through wounds animals. Infectivity may also be present in the wool or scratches on the skin (Merza and Mushi 1990). or hair of recovering animals (Kitching 2004). It is Infection by contact with lesions or infected milk is generally considered that skin scabs are the main of minor importance (Kitching 2004). Mechanical source of shed virus (Merza and Mushi 1990), and transmission is possible by the stable fly Stomoxys that infectivity may survive in scab material for at calcitrans. The virus may survive on stable flies for up least 3 months (Davies 1981). The closely related to 4 days (Mellor et al. 1987). lumpy skin disease virus has been shown to survive 18 days in dried skins (Woods 1990). The disease is regarded as being endemic in most African countries north of the equator, as well as the Middle East, Turkey, Iran, Afghanistan, and the 16.1.5. Hazard identification conclusion Indian subcontinent. In these countries transmission is facilitated by sheep and goats being herded into With the exception of the current outbreak recently crowded enclosures at night, and environmental reported in Bulgaria, all members of the European contamination leads to introduction of the virus into Union are free of sheep and goat pox. Moreover, small skin lesions. During outbreaks, the virus is transmission of capripox virus through ingestion of probably transmitted between animals by aerosols contaminated meat is not described. Capripoxvirus is (Fenner 1996). Disease occurs throughout the year, not identified as a hazard in unrestricted meat but severe outbreaks usually occur during the winter imports from the European Union. or during wet and cold weather and in animals weakened by parasites or other infections (Kitching 2004).

References

D avies FG (1981). Sheep and goat pox. In: Gibbs Kitching RP (2004). Sheep pox and goat pox. In: EPJ (ed) Virus Diseases of Food Animals, a World Coetzer JAW , Tustin RC (eds). Infectious Diseases of Geography of Epidemiology and Control, Second Edition, Livestock. Second Edition, Volume 2. Oxford Volume II, Disease Monographs. Academic Press, University Press Southern Africa, Capetown. London. Pp.733-749. Pp.1277-1281.

Fauquet CM, Mayo MA, Maniloff J, Kitching RP and Carn V (2004). Sheep pox and Desselberger U and Ball LA (2005). Virus goat pox. In: Office International des Epizooties. OIE Taxonomy. EighthReport of the International Committee on Manual o f Standards fo r Diagnostic Tests and Vaccines. Taxonomy of Viruses. Elsevier Academic Press, Fifth Edition. OIE, Paris. Pp.211-220. Amsterdam. Mellor PS, Kitching RP and Wilkinson PJ (1987). Fenner F (1996). Poxviruses. In: Fields BN, Knipe Mechanical transmission of capripox virus and DM, Howley PM (eds). Fields Virology. Third Edition. African swine fever virus by Stomoxys calcitrans. Lippincott-Raven, Philadelphia. Pp. 2697. Research in Veterinary Science 43, 109-112.

Merza M and Mushi EZ (1990). Sheep pox virus. In: Dinter Z, Morein B (eds). Virus Infections o f Ruminants. Elsevier, Amsterdam. Pp.43-51.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union OIE (2013). World Animal Health Information Woods JA (1990). Lumpy skin disease virus. In: Database (WAHID) Interface. Available at: Dinter Z, Morein B (eds). Virus Infections o f Ruminants. http: / /www.oie.int/wahis 2/public/wahid.php/Wah Elsevier, Amsterdam.pp.53-67. idhome/Home, last accessed 1 July 2103.

W illeberg P (2013). Chapter 5. Notification and animal disease surveillance. In: Risk assessments regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 17. CLASSICAL SWINE FEVER VIRUS

17.1. HAZARD IDENTIFICATION 17.1.1. Aetiological agent 17.1.3. European Union status

Classical swine fever virus (CSFV) belongs to the Table 12 (below) summarises the CSF status of the Pestivirus genus of the Flaviviridae family. It is closely 28 countries of the European Union based on their related to the ruminant pestiviruses that cause bovine official returns to the OIE. viral diarrhoea and border disease (Thiel et al. 2005).

17.1.2. Iceland status

Classical swine fever (CSF) was last reported in Iceland in 1953 and is listed as a group A notifiable disease in Act No 25/1993 (Willeberg 2013). Ongoing freedom is supported by general surveillance (OIE 2013).

Table 12: Status of classical swine fever in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported 1997 Belgium Freedom Last reported 1997 Bulgaria Freedom Last reported July 2008 Croatia Freedom Last reported May 2009 Cyprus Freedom Last reported 1967 Czech Republic Freedom Last reported 1997 Denmark Freedom Last reported 1933 Estonia Freedom Last reported January 1994 Finland Freedom Last reported 1917 France Freedom Last reported 2002 Germany Freedom Last reported November 2006 Greece Freedom Last reported July 1985 Hungary Freedom Last reported May 1993 Ireland Freedom Last reported 1958 Italy Freedom Last reported September 2003 Latvia Present Infection present in one or more zones Lithuania Freedom Last reported September 2011 Luxembourg Freedom Last reported August 2003 Malta Freedom Last reported 1967 Netherlands Freedom Last reported March 1998 Poland Freedom Last reported September 1994 Portugal Freedom Last reported 1985 Romania Freedom Last reported January 2008 Slovakia Freedom Last reported September 2008 Slovenia Freedom Last reported May 1996 Spain Freedom Last reported May 2002 Sweden Freedom Last reported 1944 United Kingdom Freedom Last reported November 2000

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 17.1.4. Epidemiology that only a few grams of tissue would be required to infect recipient pigs (MacDiarmid 1991). CSFV can remain infectious for nearly 3 months in refrigerated CSFV is the causative agent of classical swine fever meat and for more than 4 years in frozen meat (Farez (CSF), a highly contagious disease of pigs. CSF was and Morley 1997). once globally widespread. However, many countries have eradicated the disease from domestic pigs including Australia, North America, and most of 17.1.5. Hazard identification conclusion Europe. Although, since 2007, outbreaks of CSF have been reported in the European Union in CSF is recognised to be present in the European Bulgaria, France, Germany, Hungary, Romania, and Union and sporadic outbreaks have been reported Slovakia (OIE 2013), possibly as a result of infected over the last decade. Pig meat is recognised to be a wild boars transmitting the virus to farmed pigs. vehicle for the introduction of this disease so CSFV is identified as a potential hazard in pig meat and pig The pig is the only natural host for CSFV. CSF is a meat products imported from the European Union. highly contagious and economically significant disease of pigs. All excretions, secretions, and tissues 17.2. RISK ASSESSMENT of affected pigs contain virus. Transmission amongst pigs occurs mainly by the oral or oral-nasal routes via 17.2.1. Entry assessment direct or indirect contact. The virus also spreads on fomites, venereally, and by artificial insemination Ante-mortem and post-mortem inspections may not (Van Oirschot 2004). always detect pigs infected with mildly virulent strains of CSFV and those individuals that are persistently Acute, subacute, and chronic disease associated with viraemic. These animals therefore pose the highest CSFV is described. Acute CSF is characterised by risk of being infectious at slaughter and generating severe leucopaenia, haemorrhage, high fever, contaminated meat and meat products. diarrhoea, purple cyanotic discolouration of the skin, and death within 1-3 weeks. In chronic CSF, the CSFV can remain infectious for nearly 3 months in lesions are less severe but secondary bacterial refrigerated meat and for more than 4 years in frozen infections are common due to immunosuppression. meat. It does not appear to be inactivated by Pigs with chronic CSF may survive more than 3 smoking or salt curing and survives >250 days in the months before dying. In enzootic areas, many case of Iberian hams (Farez and Morley 1997; OIE chronic and clinically inapparent infections occur and 2009). Further, CSFV may survive up to 90 days in are mostly caused by virus strains of medium to low salami depending on the manufacturing process virulence (Van Oirschot 2004; Pasick 2008). (Farez and Morley 1997).

Infection of pregnant sows with CSFV strains of low The likelihood of entry of CSFV in commodities that virulence can result in the birth of immunotolerant, contain pig meat is assessed as non-negligible. persistently infected pigs, particularly when infection occurs in late gestation (Van Oirschot 2004). In pigs 17.2.2. Exposure assessment infected after birth the incubation period is 7-10 days. They are usually infective between days 5 and 14 As discussed above, CSFV most commonly enters post-infection, but can remain infective up to 3 into free countries through feeding insufficiently months in cases of chronic infections. Pigs that cooked contaminated garbage to pigs. Although recover from mild infections can carry the virus for there are a small number of commercial pig farms in long periods of time (Van Oirschot 2004). Some pigs Iceland, there has been an increase in the number of persistently infected with CSFV develop late-onset people keeping a small number of pigs as a ‘hobby’. disease with typical signs of acute or sub-acute infection after 4-6 months (Van Oirschot 2004). In addition there has been an increase in the number of sheep or cattle farms that keep a small herd of pigs. Although it is unlikely that commercial pig CSFV most commonly enters into free countries farms in Iceland would use kitchen waste as a source through feeding insufficiently cooked contaminated of feed, it is highly likely that kitchen waste would be garbage to pigs (Van Oirschot 2004). For example, used as an inexpensive source of feed for pigs in two introductions of CSF into New Zealand small hobby herds. originated through the feeding of pigs garbage from ships (Watt and Wallace 1954; Anonymous 1991). The likelihood of exposure is assessed to be non- Outbreaks of CSF have often been traced to the negligible. feeding of garbage from ships or aircraft. About 60% of CSF outbreaks in territories previously free of CSF have been attributable to importation of contaminated meat products which find their way to pigs via the practice of garbage feeding. The titre of virus reported in the muscle of infected pigs is such

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 17.2.3. Consequence assessment The virus infects pigs only. There would be no consequences for any other animals and there is no human health threat. Severity of disease would be dependent on the virulence and pathogenicity of the introduced strain. Any introduction into a naïve herd is likely to cause The consequences are assessed to be non-negligible. acute disease, which is likely to result in near 100% mortality (Anonymous 1991). 17.2.4. Risk estimation

The increasing trend in keeping small herds of pigs in Since entry, exposure, and consequence assessments Iceland has been largely driven by the domestic are non-negligible, the risk estimation is non- industry’s desire to increase the visibility of this negligible and CSFV is assessed to be a risk in species in Iceland and raise consumer awareness of unrestricted pig meat imports from the European food production. It would therefore be reasonable to Union. conclude that there is more connectivity between these hobby herds and the commercial industry in Iceland than may be seen in other countries. An outbreak of CSF in a small pig herd in Iceland is therefore likely to result in spread of disease to a large commercial herd. An outbreak of CSFV is likely to result in an effort to eradicate the disease which may include culling the entire herd.

References

Anonymous (1991). Hog cholera (Classical swine Pasick J (2008). United States Animal Health fever). Surveillance 18 (3), 16-27. Association. Classical swine fever. In Foreign Animal Diseases, Boca publications group, Boca Raton. Pp. Farez S and Morley RS (1997). Potential animal 198-205. health hazards of pork and pork products. Revue Scientifique et Technique Office International des Épizooties Thiel HJ, Collett MS, Gould EA, Heinz EX, 16, 65-78. Houghton M, Meyers G, Purcell RH, Rice CM (2005). Genus Pestivirus. In: Fauquet CM, Mayo MA, MacDiarmid SC (1991). The importation into New Maniloff J, Desselberger U, Ball LA (eds), Eighth Zealand of meat and meat products. A review of the Report o f the International Committee on Taxonomy of risks to animal health. Ministry of Agriculture and Viruses. Elsevier Academic Press, Amsterdam. Pp. Fisheries New Zealand, Wellington, New Zealand. 988-992. Available at: http: / / www.biosecurity.govt.nz/ files / regs / imports / r Van Oirschot JT (2004). Hog cholera. In: Coetzer isk/meat-meat-products-ra.pdf, last accessed 2 JAW , Tustin RC (eds.) Infectious Diseases of Livestock. September 2013. Oxford University Press, Cape Town. Pp. 975- 986.

OIE (2009). Classical swine fever (hog cholera). Technical Watt IG and Wallace GV (1954). Report of an disease card. Available at: outbreak of swine fever in Auckland. New Zealand http: / / www.oie.int/fileadmin/Home / eng/Animal Veterinary Journal 2, 7-9. Health in the World/docs/pdf/CLASSICAL SWI NE FEVER FINAL.pdf, last accessed 25 W illeberg P (2013). Chapter 5. Notification and September 2013. animal disease surveillance. In: Risk assessments regarding open trade in live animals to Iceland. Icelandic OIE (2013). World Animal Health Information Food and Veterinary Authority (MAST), Reykjavik, Database (WAHID) Interface. Available at: Iceland. Pp. 59-90. http: / /www.oie.int/wahis 2/public/wahid.php/Wah idhome/Home, last accessed 1 July 2103.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 18. CRIMEAN CONGO HAEMORRHAGIC FEVER VIRUS

18.1. HAZARD IDENTIFICATION 18.1.1. Aetiological agent 18.1.2. Iceland status

Crimean Congo haemorrhagic fever (CCHF) is Crimean Congo haemorrhagic fever (CCHF) has caused by a member of the Nairovirus genus, Crimean never been reported in Iceland. Ongoing freedom is Congo haemorrhagicfever virus (CCHFV) (Fauquet et aL supported by general surveillance (OIE 2013). 2005). 18.1.3. European Union status

Table 13 (below) summarises the CCHF status of the 28 countries of the European Union based on their official returns to the OIE.

Table 13: Status of Crimean Congo haemorrhagic fever in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Has never occurred Bulgaria Freedom Last occurrence unknown Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Has never occurred Germany Freedom Has never occurred Greece Freedom Has never occurred Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom Has never occurred Latvia Freedom Has never occurred Lithuania Freedom Last occurrence unknown Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Not reported Portugal Freedom Has never occurred Romania Not reported Slovakia Freedom Has never occurred Slovenia Freedom Has never occurred Spain Freedom Has never occurred Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 18.1.4. Epidemiology mammalian host is the usual method of transmission (Swanepoel and Burt 2004). Hyalomma spp. are the principle vectors of the disease and the distribution CCHFV infects humans and a wide variety of of the virus mirrors the distribution of these ticks ruminants and other smaller animals such as hares; it (Swanepoel et aL 1987). can also infect ostriches. In humans the virus causes a serious disease but in animals it causes a transient inapparent infection (Swanepoel and Burt 2004). The virus is relatively labile and does not survive in dried blood, at high temperatures (cooking of meat), or in a low pH environment (less than 6), and in CCHFV is principally spread by tick-bite and by matured meat (Anon 1996). contact with infected blood and meat. People involved in slaughtering animals are at risk (Swanepoel et aL 1985) and nosocomial infections 18.1.5. Hazard identification conclusion occurred in a South African hospital (Shepherd et aL 1985). The virus has been isolated from at least 30 CCHF is not present in European Union member species of ixodid ticks (Swanepoel and Burt 2004) but countries. Furthermore, transmission is principally not from argasid ticks (Durden et aL 1983). by vectors (ticks). Although contact with meat at Transovarial transmission of the virus in ticks has slaughter may lead to infection, matured meat is not a been described in a few species of the genera vehicle for the virus. CCHFV is not identified as a Rhipicephalus, Hyalomma and Dermacentor but it has hazard in unrestricted meat imports from the been suggested that this does not occur regularly and European Union. that transstadial infection following amplification in a

References

Anon (1996). Zoonoses control: Crimean-Congo Shepherd AJ, Swanepoel R, Shepherd SP, Leman haemorrhagic fever. Weekly Epidemiological Record 71, PA, Blackburn NK and Hallett AF (1985). A 381-382. nosocomial outbreak of Crimean-Congo haemorrhagic fever at Tygerberg Hospital. Part V. Durden LA, Logan TM, Wilson ML and Virological and serological observations. South African Linthicum KJ (1993). Experimental vector Medical Journal 68, 733-736. incompetence of a soft tick, Ornithodoros sonrai (Acari: Argasidae), for Crimean-Congo hemorrhagic fever Swanepoel R, Shepherd AJ, Leman PA, Shepherd virus. Journal of Medical Entomology 30, 493-496. SP and Miller GB (1985). A common-source outbreak of Crimean-Congo haemorrhagic fever on a Fauquet CM, Mayo MA, Maniloff J, dairy farm. South African Medical Journal 68, 635-637. Desselberger U and Ball LA (2005). Virus Taxonomy. Eighth Report o f the International Committee on Swanepoel R, Shepherd AJ, Leman PA, Shepherd Taxonomy of Viruses. Elsevier Academic Press, SP, McGillivray GM, Erasmus MJ, Searle LA and Amsterdam, Boston, Heidelberg, London, New York, Gill DE (1987). Epidemiologic and clinical features Oxford, Paris, San Diego, San Francisco, Singapore, of Crimean-Congo hemorrhagic fever in southern Sydney, Tokyo. Africa. American Journal of Tropical Medicine and Hygiene 36, 120-132. OIE (2013). World Animal Health Information Database (WAHID) Interface. Available at: Swanepoel R and Burt FJ (2004). Crimean-Congo http://www.oie.int/wahis 2/public/wahid.php/Wah haemorrhagic fever. In: Coetzer JAW, Tustin RC idhome/Home, last accessed 1 July 2103. (eds). Infectious Diseases o f livestock, Oxford University Press, Oxford. Pp.1077-1085.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 19. DUCK ADENOVIRUS A (EGG DROP SYNDROME)

19.1. HAZARD IDENTIFICATION 19.1.1. Aetiological agent In addition to chickens, quail are susceptible to infection and develop classical clinical signs (Das and Pradhan 1992). Although turkeys and pheasants can Egg drop syndrome is caused by duck adenovirus A, a be experimentally infected, no signs of disease are member of the genus Atadenovirus and family observed. Guinea-fowl may be naturally infected and Adenoviridae. This virus has also been known as duck develop typical signs. However, in one study, guinea- adenovirus 1 (DAdV-1), egg drop syndrome (EDS) fowl failed to show signs of disease after being virus, egg-drop-syndrome-76 (EDS-76) virus, and infected with a fowl isolate (McFerran and Smyth adenovirus 127 (McFerran and Smyth 2000; Center 2000). for Food Security and Public Health 2006)

Chicks derived from breeding flocks infected with 19.1.2. Iceland status EDSV usually remain healthy and do not produce antibody until reaching sexual maturity. Between the Egg drop syndrome has not been reported in Iceland. onset of egg laying and peak production, these individuals seroconvert and begin to lay abnormal 19.1.3. European Union status eggs (McCracken and Adair 1993). Once infection is established in a layer flock, external contamination of eggs may result in environmental contamination with Duck adenovirus A can be found worldwide in ducks EDSV leading to persistence of infection or spread and geese. Egg drop syndrome occurs in Europe, between flocks through fomites. Sporadic outbreaks Asia, Africa, and Latin America (Center for Food may also occur when chickens are exposed to EDSV Security and Public Health 2006). through contact with domestic or wild waterfowl (McFerran and Smyth 2000). 19.1.4. Epidemiology Eggs laid from infected birds show a loss of pigment Egg drop syndrome virus (EDSV) replicates in the then thin-shelled, soft-shelled or shell-less eggs may pouch shell gland and, to a lesser degree, elsewhere in be laid. Small eggs and eggs with watery albumen are the reproductive tract of infected chickens also reported. Egg production may be dramatically (Yamaguchi et al. 1981; Smyth et al. 1988). Virus reduced in an infected flock and will remain so for remains latent in birds infected before sexual maturity several weeks. Affected birds appear healthy (or in those infected as an embryo) to ensure although some workers have described inappetance transmission to the next generation (McFerran and and transient diarrhoea (McFerran and Smyth 2000). Smyth 2000). Unlike other adenoviruses, EDSV does not originate from the gastrointestinal tract, as the 19.1.5. Hazard identification conclusion virus has minimal replication in this organ (McFerran and Smyth 2000). Viral replication is restricted to the pouch shell gland and, to a lesser degree, elsewhere in the reproductive tract of infected chickens. There is no evidence to suggest EDSV is likely to be present in the meat of infected birds. EDSV is not identified as a hazard in unrestricted meat imports from the European Union.

References

Center for Food Security and Public Health McCracken RM and Adair BM (1993). (2006). Egg drop syndrome. Available at: Adenoviridae. In: Virus infection o f birds (McFerran JB http: / / www.cfsph.iastate.edu/Factsheets / pdfs/ egg and McNulty MS, eds). Elsevier Science Publishers drop syndrome.pdf , last accessed 22 September BV, Amsterdam. Pp. 123-144. 2013. McFerran JB and Smyth JA (2000). Avian Das BB and Pradhan HK (1992). Outbreaks of egg adenoviruses. Revue Scientifique et Technique Office drop syndrome due to EDS-76 virus in quail International des Épizooties 19, 589-601. (Coturnix coturnix japonica). Veterinary Record 131, 264­ 265.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Smyth JA, Platten MA and McFerran JB (1988). A study of the pathogenesis of egg drop syndrome in laying hens. Avian Pathology 17, 653-666.

Yamaguchi S, Imada T, Kawamura T, Taniguchi T and Kawakami M (1981). Pathogenicity and distribution of egg drop syndrome 1976 virus (JPA-1) in inoculated laying hens. Avian Diseases 25, 642-649.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 20. DUCK HEPATITIS VIRUS

20.1. HAZARD IDENTIFICATION 20.1.1. Aetiological agent These duck hepatitis viruses are distinct from Duck Hepatitis B Virus (DHBV), an Avihepadnavirus, which does not cause significant clinical disease in ducks Duck hepatitis is caused three different viruses; Duck (Yang et al . 2008). hepatitis virus (DHV) types 1, 2, and 3.

DHV-1 is an Avihepatovirus, a genus in the 20.1.2. Iceland status Picornaviridae family (Tseng et al. 2007). Three distinct genotypes of DHV-1 have been identified, called Duck virus hepatitis (DVH) has never been reported Duck Hepatitis A Virus (DHAV) types 1, 2, and 3 in Iceland and is listed as a group A notifiable disease (Wang et al. 2008). in Act No 25/1993 (Willeberg 2013). Ongoing freedom is supported by general surveillance (OIE DHV-2 is an Avastrovirus in the Astroviridae family 2013). (Gough et al. 1985), and has been renamed Duck Astrovirus type 1 (DAstV-1). 20.1.3. European Union status

DHV-3 is also an Avastrovirus species (Kim et al . 2008; Table 14 (below) summarises the DVH status of the Todd et al. 2009) and has been renamed Duck 28 countries of the European Union based on their Astrovirus type 2 (DAstV-2). Sequence analysis has official returns to the OIE. shown that DAstV-1 (DHV-2) and DAstV-2 (DHV- 3) are different species (Todd et al. 2009). Table 14: Status of duck virus hepatitis in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 1998 Denmark Present Disease suspected Estonia Freedom Last reported 1979 Finland Freedom Has never occurred France Not reported Germany Freedom Last occurrence unknown Greece Freedom Last occurrence unknown Hungary Freedom Last reported 2010 Ireland Not reported Italy Freedom Last occurrence unknown Latvia Freedom Last reported 1984 Lithuania Freedom Last occurrence unknown Luxembourg Freedom Last occurrence unknown Malta Freedom Has never occurred Netherlands Freedom Last reported 2004 Poland Not reported Portugal Freedom Last reported 1995 Romania Freedom Has never occurred Slovakia Freedom Last occurrence unknown Slovenia Freedom Has never occurred Spain Freedom Last occurrence unknown Sweden Freedom Has never occurred United Kingdom Freedom Last reported June 2011

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 20.1.4. Epidemiology Natural transmission of DHV occurs by the faecal- oral route (Tripathy and Hanson 1986; MingShu et al. 1997) and recovered ducks may excrete DHV in their Duck hepatitis is an acute, highly fatal, rapidly faeces for up to 8 weeks post infection (Woolcock spreading disease of young ducklings (Woolcock 2008). Spread occurs horizontally by contact with 2008). The epidemiology of DHV-1, DHV-2, and infected ducklings or fomites (Gough and McNulty DHV-3 are broadly similar. The disease has been 2008a; 2008b). Vertical transmission is not thought described in most duck-growing areas of the world to occur (Gough and McNulty 2008a). although the viruses vary in their distributions. DHAV-1 is distributed worldwide (Gough and McNulty 2008a), DHAV-2 and DHAV-3 have only The DH viruses are highly resistant to physical and been identified in Taiwan, South Korea, and China chemical conditions and are extremely stable in the (Kim et al. 2009). DAstV-1 (DHV-2) has only been environment (Koci and Schultz-Cherry 2002). The reported in the United Kingdom prior to 1985, and viruses are capable of surviving for several months DAstV-2 (DHV-3) has only been reported in the under normal environmental conditions (Gough and United States (Woolcock 2008). McNulty 2008a) and studies report survival times of 60 minutes at 50°C, 21 days at 37°C, 2 years at 4°C, and 9 years at -20°C (Woolcock 2008). DHV was DHV is extremely contagious but morbidity and inactivated after 30min at 62°C (Woolcock 2008). mortality is variable and decrease with age. Broods less than 1 week of age have 100% morbidity and mortalities as high as 95%. However, older ducklings Following natural infection, the main lesions are seen have low or negligible morbidity and mortality in the liver; which is enlarged and contains petechial although an inadequate diet increases susceptibility and ecchymotic haemorrhages; although the spleen is (Woolcock 2008). Ducklings develop age resistance sometimes enlarged and mottled and fatty kidneys from around 3 weeks and disease is rarely seen in have been described (Farmer et al. 1987; Woolcock ducklings over 4 weeks of age. Age resistance is 2008). The pathogenesis of DHV infection of ducks essentially complete from 5-6 weeks and mature is poorly understood. DHV has been detected in ducks are refractory to infection (Asplin 1958; multiple organs following experimental inoculation; Rispens 1969; Farmer et al. 1987). including liver, lung, heart, spleen, kidney, brain, muscle and pancreas (MingShu et al. 1997; Hwang and Dougherty 1974; Guerin et al. 2005, Guerin et al. Ducks are the only natural host of the DH viruses. 2007) and it has been shown to replicate in liver and Experimental infection of other species has achieved kidney cells (Haider and Calnek 1979). DHV has mixed results. Some studies failed to infect chickens been successfully transmitted to ducklings via experimentally (Reuss 1959; Schoop 1959; Hwang parenteral and aerosol inoculation with the above 1974), others reported that chicks can become tissues (Hwang and Dougherty 1974) and by oral infected and transmit infection without developing inoculation with pancreas extracts (Guerin et al. clinical signs (Asplin 1970), whilst others show high 2005). In contrast, others have failed to demonstrate mortalities (more than 50%) in a variety of non­ the presence of DHV in the spleen and muscle chicken avian species following experimental despite histological changes of these tissues inoculation (Hwang 1974). Laboratory animals are (Adamiker 1969; Adamiker 1970). refractory to infection with DHV (Reuss 1959; Woolcock 2008) but it is noted that one study reportedly demonstrated infection and subsequent 20.1.5. Hazard identification conclusion excretion of DHV-1 from brown rats (Woolcock 2008). The pathogenesis of DHV infection of ducks is poorly understood although many tissues have been There are no reports of natural infections in species shown to transmit infection by a number of routes. other than ducks and field observations indicate that The disease is recognised to be present in Denmark chickens are resistant to natural infection (Hwang and a number of other European Union countries 1974; Woolcock 2008). While concerns are have had outbreaks of disease over the last decade. repeatedly raised in the literature regarding the Therefore DHV is identified as a potential hazard in potential for wild birds to act as reservoirs of duck meat imported from the European Union. infection and incriminating them as vectors in outbreaks of DHV (Gough et al. 1985), they are not 20.2. RISK ASSESSMENT supported by serological evidence from several large scale studies which failed to demonstrate DHV in any 20.2.1. Entry assessment free-flying wildfowl of multiple species (Asplin 1970; Woolcock 2008). DHV is an acute disease of young ducklings and birds of slaughter age are generally resistant to The DH viruses are not known to have any human infection. Flocks infected with DHV are very likely health significance (Woolcock 2008). to show evidence of disease and accordingly should not be slaughtered for human consumption. However, infection of Muscovy ducklings is often

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union subclinical, which would not be detected. Recovered DHV is highly contagious, extremely stable in the birds may excrete virus in their faeces for up to 8 environment, and may survive for several months weeks without clinical signs and these birds may be of under usual environmental conditions. Natural slaughter age. Reversion to virulence has been transmission of DHV occurs by the faecal-oral route demonstrated with attenuated live virus passages in (Tripathy and Hanson 1986; MingShu et al. 1997). ducklings (Woolcock and Crighton 1979) and Therefore the likelihood of ducklings in a backyard vaccinated birds may be a source of DHV infection. flock being infected with DHV through exposure to raw duck meat, duck meat products or whole duck Considering the above, the likelihood of entry in carcases is assessed to be low. imported duck meat is assessed to be low. 20.2.3. Consequence assessment 20.2.2. Exposure assessment Duck hepatitis is an acute, highly fatal, rapidly There are a small number of large commercial poultry spreading disease of young ducklings characterised by flocks in Iceland and currently no commercial free­ hepatitis. Infection of any ducks in a backyard flocks range poultry farms. However, there are no would likely result in clinical disease. However, as commercial duck flocks in Iceland. Backyard poultry there are no commercial duck flocks in Iceland the keeping in Iceland is becoming increasingly popular overall consequences of introduction are assessed to and official data indicates over 403 poultry flocks in be negligible. Iceland with <100 hens. It is assumed that a small number of these flocks may also include ducks. Ducks are the only natural host of DHV so there Although waste food would not be used as feed in would be negligible consequences for other Iceland’s commercial poultry flocks, it is very likely commercial poultry species or human health. that waste food from domestic kitchens or bakeries might be used to feed small backyard poultry flocks. 20.2.4. Risk estimation DHV is inactivated after 30 minutes at 62°C. Therefore, the likelihood of backyard flocks being exposed to DHV from discarded cooked duck meat, As the consequence assessment is negligible, the risk duck meat products or whole duck carcases is estimate is negligible and DHV is not assessed to be a assessed to be negligible. risk in unrestricted meat imports from the European Union.

References

Adamiker D (1969). Elektronenmikroskopische Gough RE and McNulty MS (2008a). Untersuchungen zur Virushepatitis der Entenküken. Astroviridae. In Poultry Diseases, 6th Edition. Eds (Electron-microscopical studies on virus hepatitis of Pattison M, McMullin PF, Bradbury JM, Alexander ducklings) Zentralblattfür Veterinärmedizin Reihe B, 16, DJ. Elsevier/Butterworth-Heinemann Pp. 392-397. 620-636. Gough RE and McNulty MS (2008b). Adamiker D (1970). Die Virushepatitis der Picornaviridae. In Poultry Diseases, 6th Edition. Eds Entenküken im elektronenmikroskopischen Bild. Pattison M, McMullin PF, Bradbury JM, Alexander (Virus hepatitis of ducklings under the electron- DJ. Elsevier/Butterworth-Heinemann. Pp. 350-358. microscope II. Observations on the spleen and muscle) Zentralblattfür Veterinärmedizin Reihe B, 17, Gough RE, Borland ED, Keymer IF and Stuart 880-889. JC (1985). An outbreak of duck hepatitis type II in commercial ducks. Avian Pathology 14, 227-236. Asplin FD (1958). An attenuated strain of duck hepatitis virus. Veterinary Record 70, 1226-1230. Guerin JL, Noutary V, Boissieu C, Albaric O and Wyers M (2005). Viral pancreatitis and encephalitis Asplin FD (1970). Examination of sera from of Muscovy ducklings. Veterinary Record 157, 328. wildfowl for antibodies against viruses of duck plague, duck hepatitis and duck influenza. Veterinary Guerin JL, Albaric O, Noutary V and Boissieu C Record 87, 182-183. (2007). A duck hepatitis virus type I is agent of pancreatitis and encephalitis in Muscovy duckling. In Farmer H, Chalmers WSK and Woolcock PR Proceedings of the 147th American Veterinary Medicine (1987). The duck fatty kidney syndrome - an aspect Association/50th American Association o f Avian of duck viral hepatitis. Avian Pathology 16, 227-236. Pathologists Conference, 14—18 July 2007, Washington, DC, USA, Abs 4585.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Haider SA and Calnek BW (1979). In-vitro Schoop G, Staub H and Erguney K (1959). Virus isolation, propagation, and characterization of Duck hepatitis of ducks. V. Attempted adaptation of the Hepatitis Virus type-III. Avian Diseases 23, 715-729. virus to chick embryos. Monatshefte fu r Tierheilkunde 11, 99-106. Hwang J and Dougherty, E (1964). Distribution and concentration of duck hepatitis virus in Todd D, Smyth VJ, Ball NW, Donnelly BM, inoculated ducklings and chicken embryos. Avian Wylie M, Knowles NJ and Adair BM (2009). Diseases 8, 264-268. Identification of chicken enterovirus-like viruses, duck hepatitis virus type 2 and duck hepatitis virus Kim MC, Kwon YK, Joh SJ, Kwon JH and type 3 as Astroviruses. Avian Pathology 38, 21-30. Lindberg AM (2008). Differential diagnosis between type-specific duck hepatitis virus type 1 Tripathy DN and Hanson LE (1986). Impact of (DHV-1) and recent Korean DHV-1-like isolates oral immunization against duck viral hepatitis in using a multiplex polymerase chain reaction. Avian passively immune ducklings. Preventive Veterinary Pathology 37, 171-177. Medicine 4, 355-360.

Kim MC, Kim MJ, Kwon YK, Lindberg AM, Joh Tseng CH, Knowles NJ and Tsai HJ (2007). SJ, Kwon HM, Lee YJ and Kwon JH (2009). Molecular analysis of duck hepatitis virus type 1 Development of duck hepatitis A virus type 3 vaccine indicates that it should be assigned to a new genus. and its use to protect ducklings against infections. Virus Research 123, 190-203. Vaccine 27, 6688-6694. Wang L, Pan M, Fu Y and Zhang D (2008). Koci MD and Schultz-Cherry S (2002). Avian Classification of duck hepatitis virus into three astroviruses. Avian Pathology 31, 213-227. genotypes based on molecular evolutionary analysis. Virus Genes 37, 52-59. MingShu W, AnChun C and XiaoYue C (1997). Study on duck viral hepatitis - distribution and W illeberg P (2013). Chapter 5. Notification and excretion of virulent duck hepatitis virus in ducklings animal disease surveillance. In: Risk assessments and adult ducks. Chinese Journal of Veterinary Science 17, regarding open trade in live animals to Iceland. Icelandic 254-257. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90. OIE (2013). World Animal Health Information Database (WAHID) Interface. Available at: Woolcock PR (2008). Duck hepatitis. In Diseases of http://www.oie.int/wahis 2/public/wahid.php/Wah Poultry 12th Edition. Eds Saif YM, Fadly AM, Glisson idhome/Home, last accessed 1 July 2103. JR, McDougald LR, Nolan LK, Swayne DE. Blackwell Publishing. Pp. 373-384. Reuss U (1959). Virological research on duck hepatitis. Zentralblattfu r Veterinarmedizin 6, 209-248. Woolcock PR and Crighton GW (1979). Duck virus hepatitis - serial passage of attenuated virus in Rispens BH (1969). Some aspects of conbol of ducklings. Veterinary Record 105, 30-32. infectious hepatitis in ducklings. Avian Diseases 13, 417-426. Yang M, Cheng AC, Wang MS and Xing HY (2008). Development and application of a one-step real-time TaqMan RT-PCR assay for detection of duck hepatitis virus type1. Journal of Virological Methods 153, 55-60.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 21. DUCK VIRUS ENTERITIS VIRUS

21.1. HAZARD IDENTIFICATION 21.1.1. Aetiological agent Infection produces extensive haemorrhage and necrosis, although the presentation differs between age groups and species. In mature ducks, pathology Family; Herpesviridae. Subfamily; Alphaherpesvirinae. in the digestive and reproductive organs Species: Anatid Herpesvirus 1 (also known as Duck predominates and there is free blood in body cavities. Plague Herpesvirus) (Fauquet et al. 2005). In ducklings, tissue haemorrhages are less pronounced and lymphoid lesions and subcutaneous 21.1.2. Iceland status oedema of the neck are prominent (Richter and Horzinek 1993; Gough 2008; Sandhu and Metwally Duck virus enteritis (DVE) has not been reported in 2008). Species of teal (of all ages) show few gross Iceland. lesions (Wobeser 1987) as do all birds which die very rapidly (Gough 2008). 21.1.3. European Union status It is most likely that natural infection occurs through the oral or cloacal route, either by direct or indirect DVE has been reported in many countries in Europe, contact (Richter and Horzinek 1993; Gough 2008; Asia, and North America (Gough 2008). Sandhu and Metwally 2008). Virus initially replicates in the mucosa of the digestive tract, particularly the 21.1.4. Epidemiology oesophagus and cloaca, and virus then spreads to the bursa of Fabricius, thymus, spleen, liver and then to DVE is an acute (sometimes chronic) disease of other organs (Islam and Khan 1995; Shawky and waterfowl associated with high morbidity and Schat 2002; Yue et al. 2007; Gough 2008; Qi et al. mortality, and may also be referred to as duck plague, 2008; Sandhu and Metwally 2008). Virus cannot be anatid herpes, eendenpest, entenpest and peste du isolated from the muscle of infected birds (Cheng et canard (Woolcock 2012). Differences in virulence al. 2008). between viral strains have been reported but no molecular basis for these differences has been Birds that survive infection may become silent identified, although different viral subtypes are carriers and periodically shed the virus both orally recognised (Gough 2008; Sandhu and Metwally and through excreta (Richter and Horzinek 1993; 2008). Campagnolo et al. 2001; Gough 2008). Many healthy waterfowl have been found to be carriers of DVE Naturally occurring outbreaks of DVE have been (Burgess et al. 1979; Ziedler and Hlinak 1992) and reported in domestic and wild ducks, geese, and isolated cases in wild anatids, including mallards, have swans (Wobeser and Docherty 1987; Gough 2008; been reported (Wobeser and Docherty 1987). Sandhu and Metwally 2008). Natural infection has not been reported in other avian species or mammals Serious outbreaks with high mortality in migratory and transmission studies in a variety of species other waterfowl have been reported (Converse and Kidd than waterfowl have been unsuccessful (Gough 2008; 2001; Sandhu and Metwally 2008). The most Woolcock 2012). Susceptibility to infection varies devastating of these resulted in the death of over between different waterfowl species (Montgomery et 43,000 wild mallard ducks and several hundred al. 1981). Muscovy ducks and teal are highly Canada geese. Another outbreak resulted in deaths susceptible, whereas mallards appear to be resistant of over 1,400 wild waterfowl of different species and may be a possible natural reservoir of virus (Goldberg et al. 1990; Campagnolo et al. 2001). (Montgomery et al. 1981; Wobeser 1987; Campagnolo et al. 2001; Converse and Kidd 2001; Sandhu and Maternal immunity in ducklings declines rapidly Metwally 2008). (Richter and Horzinek 1993; Sandhu and Metwally 2008). Field observations suggest that recovered Flock infection usually presents as sudden, high and birds are immune to re-infection. However, persistent mortality with a significant drop in egg experimental studies have shown that superinfection production, with occasional deaths seen once of persistently infected birds may result in death infection becomes chronic (Gough 2008; Woolcock (Sandhu and Metwally 2008). 2012). The morbidity and mortality in a flock will range from 5% to 100% depending on the virulence 21.1.5. Hazard identification conclusion of the virus and the age and immunologic status of the birds (Campagnolo et al. 2001; Sandhu and Metwally 2008). DVE is most likely to affect mature Natural infection has not been reported in chickens birds (Richter and Horzinek 1993). or turkeys and DVE is not identified as a hazard in imported products derived from these species.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union There are no reports that the virus has been isolated indicates that the virus is highly infectious. DVE is in the muscle and one study failed to find virus or stable in the environment, and may survive for a viral antigen in muscle of infected birds (Cheng et aL month under usual environmental conditions. 2008). Duck virus enteritis is not identified as a Therefore the likelihood of any ducklings in a hazard in duck meat, or duck meat products. backyard flock being infected with DVE through exposure to scraps of raw duck carcases is assessed to The virus may be isolated from the liver, spleen and be low. kidneys (Islam and Khan 1995; Woolcock 2012). The kidneys are not usually removed from duck carcases during processing and therefore DVE is identified as Waterfowl of order Anseriformes are the only natural a potential hazard in whole duck carcases. host of DVE virus. Wild mallards, like many other wild waterfowl, are recognised to be silent carriers 21.2. RISK ASSESSMENT and periodic shedders of the DVE virus (Campagnolo et aL 2001). The oral dose of Guerin et 21.2.1. Entry assessment aL virus sufficient to initiate infection in wild birds is not known (Burgess et aL 1979) and an increased Flocks infected with DVE are very likely to show incidence of DVE in migratory waterfowl has not evidence of disease and accordingly should not be been observed following outbreaks in backyard flocks slaughtered for human consumption. However in the US (Montgomery et al. 1981). However the subclinically infected birds, latent carriers, or birds virus has a long outdoor survival time and the with few gross lesions may be overlooked at necropsy likelihood of free-living waterfowl being infected with (Wobeser 1987). In these birds, fragments of DVE, either following exposure to an infected infective tissues present in duck carcases after backyard duck flock, or through consumption of processing may be a source of virus. Considering the scraps from raw duck carcases, is assessed to be low. above, the likelihood of entry of DVE in imported whole duck carcases is assessed to be very low. 21.2.3. Consequence assessment

21.2.2. Exposure assessment DVE produces significant economic losses due to mortality, condemnations, and decreased egg According to Wobeser (1987), “the long term production (Sandhu and Metwally 2008). However, persistence of infection in carrier birds with periodic as there are no commercial duck farms in Iceland, the shedding of virus; transovarial transmission; ease of economic consequences of introducing DVE would transmission by a variety of routes; and relative be negligible. hardiness of the virus in surface water all suggest that infection could become widespread in nature”. Exposure of wild susceptible birds to DVE in a backyard poultry flock that included ducks could lead There are a small number of large commercial poultry to dissemination of the virus. However, the flocks in Iceland and currently no commercial free­ likelihood of wild bird exposure from a small range poultry farms. However, there are no backyard flock in Iceland is likely to be considerably commercial duck flocks in Iceland. Backyard poultry lower than the likelihood of migratory wild birds keeping in Iceland is becoming increasingly popular being exposed to DVE through exposure to other and official data indicates over 403 poultry flocks in birds (or commercial duck farms) overseas. Iceland with <100 hens. It is assumed that a small number of these flocks may also include ducks. There are no consequences for humans or species Although waste food would not be used as feed in other than waterfowl of order Anseriformes (ducks, Iceland’s commercial poultry flocks, it is very likely geese and swans). that waste food from domestic kitchens or bakeries might be used to feed small backyard poultry flocks. Reflecting the above, the consequences of DVE is inactivated after 10 minutes at 56°C therefore introducing DVE through imported meat are the likelihood of backyard flocks being exposed to assessed to be negligible. DVE in scraps from duck carcases following domestic cooking is assessed to be negligible. 21.2.4. Risk estimation It is most likely that natural infection occurs through the oral or cloacal route, either by direct or indirect As the consequence assessment is negligible, the risk contact (Richter and Horzinek 1993; Gough 2008; estimate is negligible and DVE is not assessed to be a Sandhu and Metwally 2008). The oral dose of DVE risk in unrestricted meat imports from the European sufficient to initiate infection is not known. However Union. the large numbers of birds affected in outbreaks

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union References

Burgess EC, Ossa J and Yuill TM (1979). Duck Qi X, Yang X, Cheng A, Wang M, Zhu D and Jia plague - carrier state in waterfowl. Avian Diseases 23, R (2008). The pathogenesis of duck virus enteritis in 940-949. experimentally infected ducks: a quantitative time- course study using TaqMan polymerase chain Campagnolo ER, Banerjee M, Panigrahy B and reaction. Avian Pathology 37, 307-310. Jones JL (2001). An outbreak of duck viral enteritis (duck plague) in domestic Muscovy ducks (Cairina Richter JHM and Horzinek MC (1993). Duck moschata domesticus) in Illinois. Avian Diseases 45, Plague. In Virus Infections of Birds Volume 4. Eds 522-528. McFerran JB, McNulty MS. Elsevier Science Publishers BV. Pp. 77-90. Cheng AC, Liao YH, Zhu DK, Wang MS, Yuan GP, Xu C and Han XY (2008). Replication of duck Sandhu TS and Metwally SA (2008). Duck Virus plague virus in artificially infected ducks detected by Enteritis (Duck Plague). In Diseases o f Poultry 12th in situ hybridization. Chinese Journal o f Virology 24, 72­ Edition. Eds Saif YM, Fadly AM, Glisson JR, 75. McDougald LR, Nolan LK, Swayne DE. Blackwell Publishing. Pp. 384-393. Converse KA and Kidd GA (2001). Duck plague epizootics in the United States, 1967-1995. Journal o f Shawky S and Schat KA (2002). Latency sites and Wildlife Diseases 37, 347-357 reactivation of duck enteritis virus. Avian Diseases 46, 308-313. Fauquet CM, Mayo MA, Maniloff J, Desselberger U and Ball LA (2005). Wobeser G (1987). Experimental duck plague in Herpesviridae. In Virus taxonomy. Eighth report of blue-winged teal and Canada geese. Journal of Wildlife the international committee on taxonomy of viruses. Diseases 23, 368-375. Elsevier Academic Press, California. Pp. 193-212. Wobeser G and Docherty DE (1987). A solitary Goldberg DR, Yuill TM and Burgess EC (1990). case of duck plague in a wild mallard. Journal o f Mortality from duck plague virus in Wildlife Diseases 23, 479-482. immunosuppressed adult mallard ducks. Journal o f Wildlife Diseases 26, 299-306. Woolcock PR (2012). Chapter 2.3.7. Duck virus enteritis. Manual of Diagnostic Tests and Vaccines for Gough RE (2008). Herpesviridae. In Poultry Diseases Terrestrial Animals. Available at: 6th Edition. Eds Pattison M, McMullin PF, Bradbury http: //www.oie.int/fileadmin/Home/eng/Health st JM, Alexander DJ. Elsevier/Butterworth­ andards/tahm/2.03.07 DVE.pdf, last accessed 10 Heinemann. Pp. 258-275. September 2013.

Islam MR and Khan MAHNA (1995). An Yue H, Yang FL, Jing B, Tang C and Zhang HR immunocytochemical study on the sequential tissue (2007). Quantitative study on distribution and distribution of duck plague virus. Avian Pathology 24, latency sites of duck plague virus. Chinese Journal of 189-194. Preventive Veterinary Medicine 29, 671-675.

Montgomery RD, Stein G, Novilla MN, Hurley Ziedler K and Hlinak A (1992). Investigations on SS and Fink RJ (1981). An outbreak of duck virus the incidence of virus enteritis (duck plague) in wild enteritis (duck plague) in a captive flock of mixed birds. Berliner undMunchener Tierarytliche Wochenschrift waterfowl. Avian Diseases 25, 207-213. 105, 122-125.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 22. FOOT AND MOUTH DISEASE VIRUS

22.1. HAZARD IDENTIFICATION 22.1.1. Aetiological agent 22.1.2. Iceland status

Family: Picornaviridae; Genus: Apthovirus. Foot and Foot and mouth disease (FMD) has never been mouth disease virus (FMDV). There are seven serotypes reported in Iceland and is listed as a group A of the virus: O, A, C, SAT 1, SAT 2, SAT 3 and Asia notifiable disease in Act No 25/1993 (Willeberg 1 (Paton et al. 2012). 2013). Ongoing freedom is supported by general surveillance (OIE 2013a).

22.1.3. European Union status

Table 15 (below) summarises the FMD status of the 28 countries of the European Union based on their official returns to the OIE.

Table 15: Status of foot and mouth disease in European Union countries based on their official returns to the OIE (OIE 2013a)

EU M em ber Disease status O ther Austria Freedom Last occurred April 1981 Belgium Freedom Last occurred February 1976 Bulgaria Freedom Last occurred June 2011 Croatia Freedom Last occurred 1978 Cyprus Freedom Last occurred November 2007 Czech Republic Freedom Last occurred 1975 Denmark Freedom Last occurred 1983 Estonia Freedom Last occurred December 1982 Finland Freedom Last occurred 1959 France Freedom Last occurred March 2001 Germany Freedom Last occurred January 1988 Greece Freedom Last occurred September 2000 Hungary Freedom Last occurred 1973 Ireland Freedom Last occurred March 2001 Italy Freedom Last occurred June 1993 Latvia Freedom Last occurred January 1987 Lithuania Freedom Last occurred 1982 Luxembourg Freedom Last occurred 1964 Malta Freedom Last occurred 1978 Netherlands Freedom Last occurred April 2001 Poland Freedom Last occurred 1971 Portugal Freedom Last occurred August 1984 Romania Freedom Last occurred 1973 Slovakia Freedom Last occurred 1973 Slovenia Freedom Last occurred 1968 Spain Freedom Last occurred 1986 Sweden Freedom Last occurred 1966 United Kingdom Freedom Last occurred December 2007

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 22.1.4. Epidemiology Several outbreaks in England have been attributed to imported infected meat, bones, and meat wrappers. However, since the introduction of requirements for FMD is a highly contagious viral disease that causes deboning, maturation, and a ban on all swill feeding high fever, vesicular lesions, and ulcerations. FMD is to pigs in the United Kingdom, there is no evidence considered the most contagious and economically that boneless beef imports into the United Kingdom devastating animal disease. The outbreaks of the from Argentina has led to any outbreaks of FMD. disease in Britain in 2001 (Thompson et al. 2002) and Further, no outbreaks of FMD have been attributable in Taiwan in 1997 (Yang et al. 1999) cost those to the trade in boneless beef into Europe, despite countries billions of dollars. large-scale imports from South America and smaller- scale imports from Southern Africa (Paton et al. Host species include cattle, zebus, domestic 2011). buffaloes, yaks, sheep, goats, swine, all wild ruminants, wild Suidae, and members of the Camelidae Susceptibility of FMDV to low pH (<6.0) prohibits family. Although all cloven hoofed animals are its survival in muscle following rigor mortis (USAHA susceptible, expression of disease is variable from 2008) even if cattle are slaughtered at the height of severe clinical signs to inapparent infections (Paton et viraemia. However, the required level of acidification al. 2012). Sheep may show no clinical signs whilst cannot be guaranteed under all circumstances. This is infectious, and pigs are an important amplifying host. the basis for the current requirements in the OIE Code (OIE 2013) concerning maturation and pH The incubation period ranges from 2-14 days. assessment of beef carcasses to ensure that this has Morbidity in domestic species is near 100% but is occurred. Good correlation has been found between variable in wildlife. About 15-50% of cattle become the pH level of Longissimus dorsi muscles and many carriers following infection. The virus may persist in other beef muscles of the same carcass (Paton et al. the pharyngeal region for over 3 years. The virus 2011). However, unlike beef, pig meat does not type influences the duration of the carrier state. consistently reach as low an ultimate pH during However, carriers are not epidemiologically carcass maturation. Consequently, the inactivation of important since evidence suggests that they do not FMD virus in pig meat may not be as complete as act as a source of infection (USAHA 2008). In pigs, a that in beef (Farez and Morley 1997). carrier state does not occur (Farez and Morley 1997). In contrast to muscle, other tissues and organs that The levels of virus present in animals peak at around may harbour FMDV do not undergo acidification, the time of onset of clinical signs, but significant and in these tissues the virus can survive the levels of virus may be present before this time. maturation process and subsequent low temperature FMDV infected animals may excrete virus 4 days carcass storage. These include heads, feet, viscera, prior to clinical signs appearing (Geering et al. 1995). bones, and major lymph nodes, all of which the Code recommends should be removed during the Seven immunologically distinct types of FMDV have processing of the carcass. been identified. For each virus type, immunologically related subtypes also exist, creating 60 known type­ 22.1.5. Hazard identification conclusion subtype combinations. During an infection, virus recombinations, mutations, and host selection result in the constant generation of new FMD variants, Although a number of meat and meat products may creating challenges in vaccine strain selection act as a vehicle for the introduction of FMDV, all (USAHA 2008). members of the European Union are free from this disease. FMDV is not identified as a hazard in unrestricted meat imports from the European Union. Transmission occurs by direct contact with infected animals that excrete the virus in saliva, faeces, urine, milk, semen, ocular, and nasal discharges. Infected animal products, contaminated objects, and transmission by aerosol for distances up to 60 km overland and 300 km by sea have been reported (Gloster et al. 1982).

References

Farez S and Morley RS (1997). Potential animal Geering WA, Forman AJ and Nunn MJ (1995). health hazards of pork and pork products. Review Exotic Disease of Animals: A field guide for Scientifique et Technique de l’Office Internationale des Australian veterinarians, Australian Government Epizooties 16, 65-78. Publishing Service, Canberra.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Gloster J, Sellers RF and Donaldson AI (1982). Thompson D, Muriel P, Russell D, Osborne P, Long distance spread of foot and mouth disease virus Bromley A, Rowland M, Creigh-Tyte S and over the sea. Veterinary Record 110, 47-52. Brown C (2002). Economic costs of the foot and mouth disease outbreak in the United Kingdom in OIE (2013a). World Animal Health Information 2001. Revue Scientifique et Technique Office International des Database (WAHID) Interface. Available at: Épizooties 21, 675-87. http: / /www.oie.int/wahis 2/public/wahid.php/Wah idhome/Home, last accessed 1 July 2103. USAHA (2008). United States Animal Health Association. Foot and mouth disease. In Foreign OIE (2013b). Chapter 8.5. Foot and mouth disease. Animal Diseases, Boca publications group, Boca Raton. In OIE Terrestrial Animal Health Code, OIE, Paris, Pp. 261-276. Available at: http://www.oie.int/index.php?id=169&L=0&htmfil W illeberg P (2013). Chapter 5. Notification and e=chapitre 1.8.5.htm , last accessed 6 August 2013. animal disease surveillance. In: Risk assessments regarding open trade in live animals to Iceland. Icelandic Paton D J, Sinclair M and Rodriguez R (2011). Food and Veterinary Authority (MAST), Reykjavik, Qualitative Risk Assessment of the Spread of Foot Iceland. Pp. 59-90. and Mouth Disease by International Trade in Deboned Beef. Technical Series Volume 11, OIE, Paris. Yang PC, Chu RM, Chung WB and Sung HT (1999). Epidemiological characteristics and economic Paton DJ, Barnett PV and Ferris NP (2012). costs of the foot and mouth disease epidemic in Chapter 2.1.5. Foot and mouth disease. In: OIE Taiwan. Veterinary Record 145, 731-734. Manual o f Diagnostic Tests and Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: http://www.oie.int/fileadmin/Home/eng/Health st andards/tahm/2.01.05 FMD.pdf, last accessed 1 July 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 23. INFECTIOUS BURSAL DISEASE VIRUS

23.1. HAZARD IDENTIFICATION 23.1.1. Aetiological agent 23.1.2. Iceland status

Family. Birnaviridae, Genus. Avibirnavirus. Infectious Infectious bursal disease (IBD) was last reported in bursal disease virus (IBDV) (Eterradossi and Saif 2008). Iceland in 1998 and is listed as a group B notifiable Two serotypes are recognised (IBDV-1 and IBDV-2) disease in Act No 25/1993 (Willeberg 2013). (McFerran et aL 1980). Variant and very virulent Ongoing freedom is supported by general strains of IBDV-1 (vvIBDV) are described surveillance (OIE 2013). (Rosenberger and Cloud 1986; Chettle et al. 1989). 23.1.3. European Union status

Table 16 (below) summarises the IBD status of the 28 countries of the European Union based on their official returns to the OIE.

Table 16: Status of infectious bursal disease in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 1998 Croatia Freedom Last reported May 2005 Cyprus Freedom Last reported December 2009 Czech Republic Freedom Last occurrence unknown Denmark Present Clinical disease Estonia Freedom Last occurrence unknown Finland Freedom Last reported 2006 France Nor reported Germany Present Clinical disease Greece Freedom Last occurrence unknown Hungary Present Restricted to certain zones Ireland Present Clinical disease Italy Freedom Last occurrence unknown Latvia Freedom Last reported February 1997 Lithuania Freedom Last occurrence unknown Luxembourg Freedom Has never occurred Malta Freedom Last reported 2004 Netherlands Present Clinical disease Poland Freedom Last reported September 2009 Portugal Freedom Last reported December 2011 Romania Freedom Last reported February 2005 Slovakia Freedom Last reported 2003 Slovenia Freedom Last reported August 2009 Spain Freedom Last occurrence unknown Sweden Freedom Last reported 2000 United Kingdom Present Clinical disease

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 23.1.4. Epidemiology lymphoid tissues is much lower than in the bursa and is limited to the viraemic period (Eterradossi and Saif 2008). Virus persists in the bursal tissue of IBD was first described in Gumboro, Delaware experimentally inoculated chickens for up to 3 weeks, where 10-20% of birds in infected flocks showed although this period may be shorter in infected chicks signs of diarrhoea, followed by anorexia, depression, with maternal antibodies (Abdel-Alim and Saif 2001). trembling, severe prostration, and death (Cosgrove 1962). A second viral serotype, IBDV-2, was identified in turkeys in 1980 (McFerran et al. 1980). Although there has been serological evidence of Variant strains of IBDV-1 were recognised in 1986 IBDV-1 exposure in some commercial turkey flocks, (Rosenberger and Cloud 1986) and very virulent this has been limited to flocks derived from parent strains of IBDV-1 (vvIBDV) were described in 1989 hens vaccinated with IBDV-1 vaccines (Barnes et al. (Chettle et al. 1989), which are associated with much 1982; Jackwood et al. 1982; Chin et al. 1984). A higher levels of mortality in infected flocks (Van den survey of 32 turkey flocks in England found Berg et al. 1991). antibodies against IBDV-2 in 29 flocks, while no turkey flocks had antibodies against IBDV-1, despite the widespread infection of chickens in England with IBDV-1 infections are found worldwide and in IBDV-1 (Eddy et al. 1985). Giambrone et al. (1978) countries where the virus is present the incidence is experimentally inoculated turkey poults with an high, either due to natural infection or vaccination. IBDV-1 isolate that had been passaged through In the United States, variant strains predominate, turkeys six times, in order to increase pathogenicity in whereas in Europe, Africa, Asia, and South America this species. The resulting infections were subclinical vvIBDV strains are predominant (Eterradossi and with no morbidity, mortality, or gross lesions Saif 2008). observed. However, microscopic changes were seen in the lymphoid organs of infected poults and similar Chickens are the only animals known to develop changes were seen in noninoculated poults housed clinical disease and distinct lesions when exposed to with the experimentally infected birds. Similarly, IBDV (Eterradossi and Saif 2008). Variant IBDV-1 experimental infection of turkey poults with IBDV-1 strains are associated with few clinical signs but was shown to result in microscopic changes in the marked bursal lesions, classical IBDV-1 strains are bursa of Fabricius and impairment of the immune associated with 10-50% mortality, and vvIBDV-1 system, although these changes were only partial and strains may cause 50-100% mortality in infected in no way comparable to those seen in chickens flocks (Eterradossi 2008). Although Sivanandan et al. infected with IBDV-1 (Perelman and Heller 1983). (1986) reported bursal necrosis and atrophy in specific-pathogen-free (SPF) chickens experimentally More recently, Oladele et al. (2009) experimentally infected with an IBDV-2 isolate, Ismail et al. (1988) inoculated chickens, turkeys, and ducks with IBDV-1 found that five different IBDV-2 isolates (including and found that all three species could be infected the isolate that was claimed to be used by Sivanandan with the virus, although there was no bursal damage et al. 1986) caused no gross or microscopic lesions in and minimal viral replication in ducks and turkeys. SPF chickens and had no significant impact on bursa- The authors concluded that the chicken host has a to-body-weight ratio when compared to uninfected facilitating inherent ‘factor’ which permits maximal controls. replication of IBDV, compared with turkeys and ducks. Chickens are most susceptible to infection with IBDV between 3 and 6 weeks of age. Infection is Experimental infection of day-old turkey poults with followed by a short incubation period with clinical IBDV-2 results in no clinical disease or histological signs seen 2-3 days after exposure (Eterradossi and changes in the bursa, spleen, or thymus, although Saif 2008). Following infection, the bursa is the suppression of the cellular immune system and a primary target organ of the virus, with marked decrease in the plasma cell population of the oedema and hyperaemia seen 3 days after infection Harderian gland have been described (Nusbaum et al. (Cheville 1967). Microscopic lesions are seen in the 1988). lymphoid tissues with the most marked changes (degeneration and necrosis) being described in the cloacal bursa (Cheville 1967; Mandelli et al. 1967; Homogenates of bursa, muscle, skin, and fat taken Peters 1967) whilst other histopathological changes from 4-week-old chickens infected with vvIBDV have been noted in the spleen, thymus, caecal tonsils, have been shown to infect 3-week-old recipients kidney, and liver (Helmboldt and Garner 1964), and when given orally. Following challenge of 3-week- also in the Harderian gland (Dohms et al. 1981). old chickens with vvIBDV, infectious virus was demonstrated in the liver, kidney, faeces, bursa, and blood 24-96 hours after infection and in muscle Following oral infection of chickens with IBDV, homogenates at 48, 72, and 96 hours post infection. virus can be found in the liver after 5 hours and then The viral titre in muscle was found to peak at 10117 progresses to other tissues including the bursa. median chick infective doses (CID50) per gram, 3 Following this initial bursal infection there is a second days post-infection. Pools of muscle, liver, kidney, massive viraemia although the peak viral titre in non­

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union spleen, lung, and bursa harvested at 4, 7, 9, 11, 16, 18, domestic poultry consumption is imported from and 21 days post-infection with IBDV-1 were all overseas then the introduction of virus would be infectious to 3-week-old SPF chickens when given virtually certain (MAF 1999). orally (MAF 1999). Reflecting the above, the entry assessment for IBDV 23.1.5. Hazard identification conclusion in chicken meat is assessed to be high.

Infection with IBDV-2 is not associated with any 23.2.2. Exposure assessment clinical disease in turkeys or experimentally infected chickens, and there are no reports of IBDV-2 causing There are a small number of large commercial poultry disease in free-living avian species. There would be flocks in Iceland and currently no commercial free­ little justification for applying sanitary measures for range poultry farms. Backyard poultry keeping in IBDV-2 to the international trade in poultry meat. Iceland is becoming increasingly popular and official The available evidence suggests that IBDV-1 should data indicates over 403 poultry flocks in Iceland with not be considered as a hazard likely to be associated <100 hens. Although waste food would not be used with turkey or duck meat, although trade in chicken as feed in Iceland’s commercial poultry flocks, it is meat should be considered a potential vehicle for the very likely that waste food from domestic kitchens or spread of IBDV-1 (Cobb 2011). bakeries might be used to feed small backyard poultry flocks. Heat inactivation studies have shown that IBD is present in several European Union countries. there is a high probability that IBDV would survive at IBDV-1 is identified as a potential hazard in chicken infectious titres in domestically cooked chicken, meat and chicken meat products imported from the especially in deep tissues (MAF 1999), so viable European Union. IBDV is likely to be present if waste food contains raw or cooked chicken meat imported from the 23.2. RISK ASSESSMENT European Union. 23.2.1. Entry assessment The likelihood of backyard flocks being exposed to IBDV in either raw or cooked imported chicken meat As already discussed, homogenates of bursa, muscle, is assessed to be non-negligible. skin, and fat taken from 4-week-old chickens infected with vvIBDV have been shown to infect 3-week-old recipients when given orally. Following challenge of Although surveys of avian wildlife have found evidence of seroconversion to IBDV in rooks and 3-week-old chickens with vvIBDV, infectious virus was demonstrated in the liver, kidney, faeces, bursa, wild pheasants (Campbell 2001) as well as in birds of and blood 24-96 hours after infection and in muscle the family Accipitridae (hawks, eagles, kites, harriers, and Old World vultures) (Hofle et al. 2001), homogenates at 48, 72, and 96 hours post infection. experimental studies have shown that IBDV is highly The viral titre in muscle was found to peak at 101.17 host-specific and is probably not an infectious disease median chick infective doses (CID50) per gram, 3 for the majority of avian species other than the days post-infection. Pools of muscle, liver, kidney, chicken (Van den Berg et al. 2001). Therefore, the spleen, lung, and bursa harvested at 4, 7, 9, 11, 16, 18, likelihood of free-living avian species being infected and 21 days post-infection with IBDV-1 were all infectious to 3-week-old SPF chickens when given with IBDV, either following exposure to an infected backyard flock or through consumption of kitchen orally (MAF 1999). waste disposed of at sites accessible to susceptible wild avian species is assessed to be very low. More recently, research commissioned by the Australian government concluded that vvIBDV (strain CS88) can be ‘transmitted with ease from both Commercial poultry farms in Iceland are unlikely to muscle and bursa of infected non-immune chickens feed waste food and there are no commercial free­ range poultry flocks in Iceland. Commercial poultry to day-old chicks by a natural route of infection’. flocks in Iceland have a high standard of biosecurity This report further concluded that, while vaccination using standard European vaccination regimes was and there is a negligible likelihood of significant sufficient to prevent overt illness, it ‘did not inhibit contact between commercial flocks and backyard chickens from developing IBD infection when flocks. Although wild birds have been shown to challenged with vvIBDV. Sufficient virus was present seroconvert following exposure to IBDV, there are in both bursae and muscles to infect susceptible day- no reports of natural productive infection in wild old-chicks via a natural route’ (Biosecurity Australia birds with this virus. The likelihood of commercial 2008). poultry in Iceland being exposed to IBDV through imported chicken meat is assessed to be negligible.

Previous published quantitative models of the likelihood of IBDV introduction in chicken meat (MAF 1999) have concluded that, in countries free from IBD, if only a very small proportion of

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 23.2.3. Consequence assessment infected flocks (Eterradossi 2010). However, chickens are most susceptible to infection between 3 and 6 weeks of age, and mature birds in a backyard Chickens are the only animals known to develop flock would be likely to resistant to infection. Clinical clinical disease and distinct lesions when exposed to disease is unlikely in birds more than 15 to 20 weeks IBDV (Eterradossi and Saif 2008). Although there is old (Van den Berg et aL 2000). Reflecting this, the serological evidence that wild birds may be infected consequence of infection in a backyard poultry flock with IBDV, the consequences of infection in wild are assessed to be negligible. birds are assessed to be negligible.

Infection of backyard poultry flocks with IBDV may 23.2.4. Risk estimation result in mortality within that flock. Classical IBDV- 1 strains are associated with 10-50% mortality in Since the consequence assessment is assessed to be infected flocks, variant IBDV-1 strains are associated negligible, the risk is estimated to be negligible and with few clinical signs but marked bursal lesions, and IBDV is not assessed to be a risk in unrestricted meat vvIBDV-1 strains may cause 50-100% mortality in imports from the European Union.

References

Abdel-Alim GA and Saif YM (2001). Detection Cobb SP (2011). The spread of pathogens through and persistence of infectious bursal disease virus in trade in poultry meat: overview and recent specific pathogen-free and commercial broiler developments. In Disease transmission through chickens. Avian Diseases 45, 646-654. international trade (MacDiarmid S, ed.). Revue Scientifique et Technique Office International des Épiyooties Barnes HJ, Wheeler J and Reed D (1982). 30, 149-164. Serologic evidence of infectious bursal disease virus infection in Iowa turkeys. Avian Diseases 26, 560-565. Cosgrove AS (1962). An apparently new disease of chickens — avian nephrosis. Avian Diseases 6, 385-389. Biosecurity Australia (2008). Generic import risk analysis report for chicken meat. Final report. Part C. Dohms JE, Lee KP and Rosenberger JK (1981). Available at: Plasma cell changes in the gland of Harder following http://www.daff.gov.au/ data/assets/pdf file/000 infectious bursal disease virus infection of the 4/872788/2008 33c.pdf, last accessed 25 September chicken. Avian Diseases 25, 683-695. 2013. Eddy RK, Chettle NJ and Wyeth PJ (1985). Campbell (2001). Investigation into evidence of Serological survey of the incidence of infectious exposure to infectious bursal disease virus (IBDV) bursal disease serotypes 1 and 2 in chicken and turkey and chick infectious anaemia virus (CIAV) in wild flocks in England. Veterinary Record 117, 415. birds in Ireland. II. International symposium on infectious bursal disease and chicken infectious anaemia, Eterradossi N (2008). Chapter 2.3.12. Infectious Rauischholyhausen, Germany, 16-20 June 2001, 230-235. bursal disease (Gumboro disease). In: OIE Manual o f Diagnostic Tests and Vaccines fo r Terrestrial Animals, OIE, Chettle N, Stuart JC and Wyeth PJ (1989). Paris. Available at: Outbreak of virulent infectious bursal disease in East http: //www.oie.int/fileadmin/Home/eng/Health st Anglia. Veterinary Record 125, 271-272. andards/tahm/2.03.12 IBD.pdf. last accessed 1 July 2013. Cheville NF (1967). Studies on the pathogenesis of Gumboro disease in the bursa of Fabricius, spleen Eterradossi N and Saif YM (2008). Infectious and thymus of the chicken. American Journal of bursal disease. In Diseases o f Poultry 12th Edition, 2008, Pathology 51, 527-551. Ed Saif YM, Blackwell Publishing. Pp. 185-208.

Chin RP, Yamamoto R, Lin WQ, Lam KM and Giambrone JJ, Fletcher OJ, Luckert PD, Page Farver TB (1984). Serological survey of infectious RK and Eidson CE (1978). Experimental infection bursal disease virus serotypes 1 and 2 in California of turkeys with infectious bursal disease virus. Avian turkeys. Avian Diseases 28, 1026-1036 Diseases 22, 451-458.

Helmboldt CF and Garner E (1964). Experimentally induced Gumboro disease (IBA). Avian Diseases 8, 561-575.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Hofle U, Blanco JM , Kaleta EF (2001). Oladele OA, Adene DF, Obi TU and Nottidge Neutralising antibodies against infectious bursal HO (2009). Comparative susceptibility of chickens, disease virus in sera of free-living and captive birds of turkeys and ducks to infectious bursal disease virus prey from central Spain (preliminary results). II. using immunohistochemistry. Veterinary Research International symposium on infectious bursal disease and Communications 33, 111-121. chicken infectious anaemia, Rauischholzhausen, Germany, 16­ 20 June 2001, 247-251. Perelman B and Heller ED (1983). The effect of infectious bursal disease virus on the immune system Ismail NM, Saif YM and Moorhead PD (1988). of turkeys. Avian Diseases 27, 66-76. Lack of pathogenicity of five serotype 2 infectious bursal disease viruses in chickens. Avian Diseases 32, Peters G (1967). Histology of Gumboro disease. 757-759. Berliner und Münchener Tierärytüche Wochenschrift 80, 394­ 396. Jackwood DJ, Saif YM and Hughes JH (1982). Characteristics and serological studies of two Rosenberger JK and Cloud SS (1986). Isolation serotypes of infectious bursal disease virus in turkeys. and characterization of variant infectious bursal Avian Diseases 26, 871-882. disease viruses. Journal of the American Veterinary Medical Association 189, 357. MAF (1999). Import risk analysis: chicken meat and chicken meat products; Bernard Matthews Foods Ltd turkey Sivanandan V, Sasipreeyajan J, Halvorson DA meat preparations from the United Kingdom. MAF and Newman JA (1986). Histopathologic changes Regulatory Authority, New Zealand. Available at: induced by serotype II infectious bursal disease virus http: / / www.biosecurity.govt.nz / files / regs / imports / r in specific-pathogen-free chickens. Avian Diseases 30, isk/chicken-meat-ra.pdf, last accessed 14 August 709-715. 2013. Van den Berg TP, Gonze M and Meulemans G Mandelli G, Rinaldi A, Cerioli A and Cervio G (1991). Acute infectious bursal disease in poultry: (1967). Aspetti ultrastrutturali della borso di Fabrizio Isolation and characterization of a highly virulent nella malattia di Gumboro de pollo. Atti Società strain. Avian Pathology 20, 133-143. Italiana di Scienye Veterinarie 21, 615-619. Van den Berg TP, Eterradossi N, Toquin D and McFerran JB, McNulty MS, McKillop ER, Meulmans G (2000). Infectious bursal disease Connor TJ, McCracken RM, Collins DS and (Gumboro disease). Revue Scientifique et Technique Office Allan GM (1980). Isolation and serok gical studies International des Épiyooties 19, 527-543. with infectious bursal disease viruses from fowl, turkey and duck: Demonstration of a second Van den Berg TP, Ona A, Morales D and serotype. Avian Pathology 9, 395-404. Rodriguez JF (2001). Experimental inoculation of game/ornamental birds with a very virulent strain of Nusbaum KE, Lukert PD and Fletcher OJ IBDV. II. International symposium on infectious bursal (1988). Experimental infections of one-day-old disease and chicken infectious anaemia, Rauischholzhausen, poults with turkey isolates of infectious bursal disease Germany, 16-20 June 2001, 236-246. virus. Avian Pathology 17, 51-62. W illeberg P (2013). Chapter 5. Notification and OIE (2013). World Animal Health Information animal disease surveillance. In: Risk assessments Database (WAHID) Interface. Available at: regarding open trade in live animals to Iceland. Icelandic http: / /www.oie.int/wahis 2/public/wahid.php/Wah Food and Veterinary Authority (MAST), Reykjavik, idhome/Home, last accessed 1 July 2103. Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 24. NEWCASTLE DISEASE VIRUS

24.1. HAZARD IDENTIFICATION 24.1.1. Aetiological agent The Code (OIE 2013b) defines ND as an infection of poultry caused by a virus (NDV) of avian paramyxovirus serotype 1 (APMV-1) that meets one Family: Paramyxoviridae, Subfamily: Paramyxovirinae, of the following criteria for virulence: Genus: Avulavirus (Alexander and Senne 2008). Nine serogroups of avian paramyxoviruses are recognised, APMV-1 to APMV-9. Newcastle disease (ND) is i. the virus has an intracerebral caused by viruses belonging to serogroup APMV-1. pathogenicity index (ICPI) in day-old chicks (Gallusgallus) of 0.7 or greater; or Traditionally APMV-1 viruses were classified based on their pathogenicity to chicken embryos following ii. multiple basic amino acids have been allantoic inoculation. Velogenic strains of APMV-1 demonstrated in the virus (either directly caused mortality after less than 60 hours, mesogenic or by deduction) at the C-terminus of the strains caused mortality between 60 and 90 hours, F2 protein and phenylalanine at residue and lentogenic strains caused mortality after more 117, which is the N-terminus of the F1 than 90 hours (Alexander and Senne 2008). protein. The term ‘multiple basic amino Alternative pathogenicity tests assess clinical signs or acids’ refers to at least three arginine or death in infected birds (the intracerebral lysine residues between residues 113 and pathogenicity index (ICPI) in day-old chicks or the 116. Failure to demonstrate the intravenous pathogenicity index (IVPI) in six-week- characteristic pattern of amino acid old chickens) (Alexander 1988a; Afonso et al. 2012). residues as described above would require characterisation of the isolated virus by an ICPI test. Viral entry into a host cell is enabled by a viral protein (the fusion protein) fusing with the host cell membrane. During viral replication a precursor 24.1.2. Iceland status glycoprotein is produced which then has to be cleaved into the fusion protein for the progeny virus Newcastle disease has never been reported in Iceland to be infectious (Rott and Klenk 1988). The and is listed as a group A notifiable disease in Act No structure of the precursor glycoprotein cleavage site 25/1993. Surveys for Newcastle disease have been determines virus pathogenicity; virulent strains have a carried out since 1993 and systematic surveillance has cleavage site containing multiple basic amino acids, been undertaken since 2008 (Willeberg 2013). which can be cleaved by a wide range of host Ongoing freedom is supported by general and proteases enabling these strains to replicate in many targeted surveillance (OIE 2013a). different cell types, whereas low virulence strains have fewer basic amino acids in the cleavage site so are cleaved by a more limited range of host enzymes 24.1.3. European Union status and their replication is limited to the intestinal tract (Alexander and Senne 2008). The amino acid Table 17 (below) summarises the ND status of the 28 sequence of this precursor glycoprotein cleavage site countries of the European Union based on their is now considered to be an excellent guide to real or official returns to the OIE. potential virulence of viral isolates (Alexander and Senne 2008), although other factors have been described that influence viral virulence (Huang et al. 2004; Römer-Oberdörfer et al. 2006).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 17: Status of Newcastle disease in European Union countries based on their official returns to the OIE (OIE 2013a)

EU Member Disease status O ther Austria Freedom Last reported in domestic birds 1997; Reported in wild birds December 2011 Belgium Freedom Last reported August 2010 Bulgaria Freedom Last reported September 2009 Croatia Freedom Last reported December 2011 Cyprus2O0u13tb Outbreak r e a k reported June Previously last reported in domestic birds December 2006; Reported in wild birds October 2008 Czech Republic Present Disease restricted to certain zones (domestic birds) Denmark Freedom Last reported October 2005 Estonia Freedom Last reported 2007 Finland Freedom Last reported June 2012 France Freedom Last reported December 2010 Germany Freedom Last reported June 2010 Greece Freedom Last reported December 2007 Hungary Present Disease restricted to certain zones (wild birds) Ireland Freedom Last reported March 1997 Italy Present Disease restricted to certain zones (domestic and wild birds) Latvia Freedom Last reported 2006 Lithuania Freedom Last reported 1989 Luxembourg Freedom Last reported November 1999 Malta Freedom Last reported 1993 Netherlands Freedom Lest reported in domestic birds December 2010; Reported in wild birds 1996 Poland Freedom Last reported 1974 Portugal Present No clinical disease (in wild birds) Romania Freedom Last reported February 2009 Slovakia Freedom Last reported in domestic birds March 2007; Reported in wild birds 2005 Slovenia Freedom Last reported in domestic birds 1991; Reported in wild birds December 2011 Spain Present Disease restricted to certain zones (wild birds) Sweden Freedom Last reported March 2011 United Kingdom Freedom Last reported in domestic birds 2006; Reported in wild birds 2004

24.1.4. Epidemiology chickens with viscerotropic velogenic strains of APMV-1. Neurotropic velogenic strains replicate in the myocardium, air sac, and central nervous system. The vast majority of, if not all, birds are susceptible Mesogenic viral strains replicate in the myocardium, to infection with APMV-1, but the disease seen with air sac, and (rarely) in splenic macrophages. Infection any specified strain of virus may vary considerably with lentogenic isolates results in minimal transient with host (Alexander and Senne 2008). viral replication confined to the air sac at 5 days post­ exposure and myocardium at 5 and 10 days post­ The spread of infection from one bird to another is exposure (Brown et aL 1999). thought to be primarily via aerosols or large droplets although the evidence to support this is lacking Birds slaughtered for meat during disease episodes (Alexander and Senne 2008). Large amounts of virus may represent an important source of virus. Most are excreted in the faeces of an infected bird and this organs and tissues have been shown to carry is thought to be the main method of spread for infectious virus at some time during infection with enteric infections (Alexander et aL 1984). virulent NDV (Alexander 1988b). Infected meat has been shown to retain viable virus for over 250 days at Widespread viral replication occurs in the spleen, -14 to -20°C (Alexander and Senne 2008) and caecal tonsil, intestinal epithelium, myocardium, lung, dissemination by frozen meat has been described and bursa following challenge of four-week-old historically as an extremely common event (Lancaster

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 1966). Although modern methods of poultry carcase that the virus remained viable in buried poultry preparation, and legislation on the feeding of carcases for 121 days. untreated swill to poultry, have greatly diminished the risk from poultry products, the possibility of spread Kaleta and Baldauf (1988) concluded that the wealth in this way nevertheless remains (Alexander 2000). of reports on ND in free-living birds suggested that virtually all avian species are susceptible to infection 24.1.5. Hazard identification conclusion although, of the 8,000 known avian species, only 236 (2.5%) had a record of NDV isolation. Since that publication, there has been an increase in the number Poultry meat and meat products are recognised as a of species from which NDV has been recovered vehicle for the introduction of NDV. This disease is which led Alexander and Senne (2008) to conclude present in a number of European Union countries so that the vast majority of, if not all, birds are NDV is identified as a potential hazard in poultry susceptible to NDV infection. meat and meat products imported from the European Union. The likelihood of free-living avian species being infected with NDV, either following exposure to an 24.2. RISK ASSESSMENT infected backyard flock or through consumption of 24.2.1. Entry assessment uncooked poultry meat in kitchen waste disposed of at sites accessible to susceptible wild avian species is Historically, Lancaster (1966) stated that poultry assessed to be non-negligible. carcases and offal have been as great a source of NDV as live poultry and have often carried the 24.2.3. Consequence assessment disease from one country to another.

Commercial poultry farms in Iceland are unlikely to More recently, MAF (1999) reviewed studies that feed waste food and there are no commercial free­ showed the NDV titre in muscle of infected chickens range poultry flocks in Iceland. Commercial poultry was about 104 EID 50 (50% egg infectious doses) per flocks in Iceland have a high standard of biosecurity gram and the oral infectious dose of NDV in a three- and there is a negligible likelihood of significant week-old chicken was found to be 104 EID50, whilst contact between commercial flocks and backyard another study demonstrated that tissue pools of flocks. Commercial poultry flocks are therefore muscle, liver, spleen, lung, kidney and bursa collected unlikely to be exposed to NDV if it were to be at 2, 4, 7, and 9 days post-infection were infectious introduced into a small backyard flock in Iceland. for 3-week-old birds. On the basis of these studies, it However, given the variety of free-living avian was concluded that poultry meat is a suitable vehicle species that are known to be susceptible to NDV for the spread of NDV and that poultry can be infection, the establishment of NDV in wild birds in infected by the ingestion of uncooked contaminated Iceland would result in a very low likelihood of meat scraps. introducing infection into a commercial flock. The introduction of NDV would have serious The likelihood of entry of NDV is assessed to be consequences for the poultry industry and could non-negligible. result in substantial mortalities in wild and/or caged birds. 24.2.2. Exposure assessment There are reports indicating that both velogenic and There are a small number of large commercial poultry vaccine strains of APMV-1 from poultry can cause flocks in Iceland and currently no commercial free­ disease in humans (Yakhno et al. 1990; Capua and range poultry farms. Backyard poultry keeping in Alexander 2004; Alexander and Senne 2008). Iceland is becoming increasingly popular and official APMV-1 infections in humans have most commonly data indicates over 403 poultry flocks in Iceland with been reported in association with conjunctivitis, but <100 hens. Although waste food would not be used some reports have referred to chills, headaches, and as feed in Iceland’s commercial poultry flocks, it is fever. very likely that waste food from domestic kitchens or bakeries might be used to feed small backyard poultry The consequences of NDV introduction are assessed flocks. NDV may be regarded as heat labile and to be non-negligible. studies have shown that it is likely to be inactivated by domestic cooking (Alexander and Manvell 2004) 24.2.4. Risk estimation so there would be a negligible likelihood of backyard poultry being exposed to NDV from scraps of Since entry, exposure, and consequence assessments cooked poultry meat. However, NDV can persist in are non-negligible, the risk estimation is non- uncooked tissues for prolonged periods and Lancaster (1966) cited a study which demonstrated negligible and NDV is assessed to be a risk in unrestricted poultry meat imports from the European Union.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union References

Afonso CL, Miller PJ, Grund Ch, Koch G, Peeters Kaleta EF and Baldauf C (1988). Newcastle B, Selleck W and Srinivas GB (2012). Chapter disease in free-living and pet birds. In Developments in 2.3.14. Newcastle disease. In: OIE Manual of Diagnostic Veterinary Virology. Newcastle Disease. Ed Alexander Tests and Vaccines fo r Terrestrial Animals, OIE, Paris. DJ, Kluwer Academic Publishers. Pp. 197-246. Available at: http://www.oie.int/fileadmin/Home/eng/Health st Lancaster JE (1966). Newcastle disease. A review of andards /tahm/2.03.14 NEWCASTLE DIS.pdf, last some of the literature published between 1926 and 1964. accessed 1 July 2013. Monograph No. 3, Canada Department of Agriculture, Ottawa. Alexander DJ (1988a). Newcastle disease diagnosis. In Alexander DJ (ed) Newcastle disease. Kluwer MAF (1999). Import risk analysis: chicken meat and Academic Publisher, Boston, MA. Pp. 147-160. chicken meat products; Bernard Matthews Foods Ltd turkey meat preparations from the United Kingdom. MAF Alexander DJ (1988b). Newcastle disease: Methods Regulatory Authority, New Zealand. Available at: of spread. In Developments in Veterinary Virology. http: / / www.biosecurity.govt.nz / files / regs / imports / r Newcastle Disease. Ed. Alexander DJ, Kluwer isk/chicken-meat-ra.pdf. last accessed 25 September Academic Publisher, Boston, MA. Pp. 256-272. 2013

Alexander DJ (2000). Newcastle disease and other OIE (2013a). World Animal Health Information avian paramyxoviruses. Revue Scientifique et Technique Database (WAHID) Interface. Available at: Office International des Épizooties. 19, 443-462. http://www.oie.int/wahis 2/public/wahid.php/Wah idhome/Home, last accessed 1 July 2103. Alexander DJ, Parsons G and Marshall R (1984). Infection of fowls with Newcastle disease virus by OIE (2013b). Chapter 10.9 Newcastle disease. In food contaminated with pigeon faeces. Veterinary Terrestrial Animal Health Code, OIE Paris. Available at: Record 115, 601-602. http://www.oie.int/index.php?id=169&L=0&htmfil e=chapitre 1.10.9.htm, last accessed 6 August 2013. Alexander DJ and Manvell RJ (2004). Heat inactivation of Newcastle disease virus (strain Herts Römer-Oberdörfer A, Veits J, Werner O and 33/56) in artificially infected chicken meat Mettenleiter TC (2006). Enhancement of homogenate. Avian Pathology 33, 222-225. pathogenicity of Newcastle disease virus by alteration of specific amino acid residues in the surface Alexander DJ and Senne DA (2008). Newcastle glycoproteins F and HN. Avian Diseases 50, 259-263. disease, other avian paramyxoviruses, and pneumovirus infections. In Diseases o f Poultry 12th Rott R and Klenk HD (1988). Molecular basis of Edition. Ed Saif YM, Blackwell Publishing. Pp. 75­ infectivity and pathogenicity of Newcastle disease 115. virus. In Alexander DJ (ed) Newcastle disease. Kluwer Academic Publisher, Boston, MA Pp. 98-112. Brown C, King DJ and Seal BS (1999). Pathogenesis of Newcastle disease in chickens W illeberg P (2013). Chapter 5. Notification and experimentally infected with viruses of different animal disease surveillance. In: Risk assessments virulence. Veterinary Pathology 36, 125-132. regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Capua I and Alexander DJ (2004). Human health Iceland. Pp. 59-90. implications of avian influenza viruses and paramyxoviruses, European Journal of Clinical Yakhno MA, Govorkova EA, Kubinova I e t al. Microbiology and Infectious Diseases 23, 1-6. (1990). The source of avian paramyxoviruses isolated during an outbreak of influenza among children, A cta Huang ZH, Panda A, Elankumaran S, Virologica 34, 184-187. Govindarajan D, Rockemann DD and Samal SK (2004). The hemagglutinin-neuraminidase protein of Newcastle disease virus determines tropism and virulence. Journal of Virology 78, 4176-4184.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 25. NIPAH VIRUS

25.1. HAZARD IDENTIFICATION 25.1.1. Aetiological agent 25.1.2. Iceland status

Nipah virus (NiV) is a paramyxovirus in the subfamily Nipah virus encephalitis has never been reported in Paramyxovirinae, and is classified in the new genus Iceland. Ongoing freedom is supported by general Henipavirus (Eaton et aL 2006; Wang et aL 2012). surveillance (OIE 2013).

25.1.3. European Union status

Table 18 (below) summarises the Nipah virus encephalitis status of the 28 countries of the European Union based on their official returns to the OIE.

Table 18: Status of Nipah virus encephalitis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Has never occurred Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Has never occurred Germany Freedom Has never occurred Greece Freedom Last occurrence unknown Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom Has never occurred Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Not reported Portugal Freedom Has never occurred Romania Freedom Has never occurred Slovakia Freedom Has never occurred Slovenia Freedom Has never occurred Spain Freedom Has never occurred Sweden Freedom Has never occurred United Kingdom Freedom Last occurrence unknown

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 25.1.4. Epidemiology Virus isolation of NiV from unfixed samples followed by identification procedures such as immunostaining, serum neutralisation, or molecular Nipah virus is a rare tropical disease, first reported in characterisation are described. Real-time polymerase Malaysia in 1998 and subsequently in Singapore, chain reaction is also available as a diagnostic test. Bangladesh, and India (Tan and Wong 2003; Katu Immunohistochemistry of fixed tissue can also be 2004; Epstein et al. 2006). The disease appears used to detect NiV antigens. Virus neutralisation sporadically in tropical climates where the natural tests and enzyme-linked immunosorbent assays are reservoir host Pteropid fruit bat species are found. also available for serological diagnosis of NiV infection (Daniels et al. 2008). Infected pigs excrete the virus in urine and respiratory droplets and virus is not excreted by pigs Virus spread between farms is usually associated with once neutralising antibodies appear 14-18 days post­ pig movements (Center for Food Security and Public infection (Middleton et al. 2002). Chronic infections Health 2007). Natural infection of pigs with NiV do not appear to be a feature of the disease. leads to lesions in both the brain and lungs of an individual with tracheitis, pneumonia, and Direct, close contact with pigs was the primary meningoencephalitis described. The lungs and source of a major public health crisis, with the death meninges are recognised as the most important target of 105 people, when NiV first appeared (Katu 2004). organs following experimental infection with vascular The virus attacks the central nervous system and degeneration also described in the gastric submucosa respiratory systems of humans, leading to death due and muscle, ureteral submucosal, spleen, and hepatic to encephalitis. The movement of infected pigs from arterioles. The spread of NiV from infected pigs is Malaysia to an abattoir in Singapore resulted in principally through coughed-up sputum and expired encephalitis in 35 abattoir workers with confirmed air, with excretion also possible via the placenta NiV infection in 11 of these (Paton et al. 1999; Chua (Hooper et al. 2001). et al. 2000). There is little information on the presence of NiV in Five outbreaks of NiV were described in Bangladesh pig meat and eating pig meat during the Malaysian between 2001 and 2005, involving much smaller epidemic was not implicated as a source of infection. numbers of affected humans and no animal disease. Moreover NiV has not been described in any These outbreaks appear to have been due to spillover European Union member states. of virus directly from bats to humans (Epstein et al. 2006). One outbreak was reported in 2001 in India, close to the Bangladesh border (Chadha et al. 2006). 25.1.5. Hazard identification conclusion Since 2001, almost annual human outbreaks of fatal encephalitis caused by NiV in Bangladesh and There is no evidence to suggest NiV is likely to be sporadic outbreaks in India have been reported. associated with pig meat or pig meat products. The Although human-to-human transmission was not geographically limited distribution of this virus means seen in the Malaysia and Singapore outbreak, recent that it is not identified as a hazard in unrestricted outbreaks in Bangladesh have led to the suspicion of meat imports from the European Union. human-to-human and foodborne transmission of NiV (Lo et al. 2012). The threat to human health is significant since NiV infection has a high mortality rate of 33-75% recorded in different outbreaks (Center for Food Security and Public Health 2007).

References

Center for Food Security and Public Health Chua KB, Bellini WJ, Rota PA, Harcourt BH, (2007). Nipah virus infection. Available at: Tamin A, Lam SK, Ksiazek TG, Rollin PE, Zaki http: / / www.cfsph.iastate.edu/Factsheets/pdfs/ nipah SR, Shieh W-J, Goldsmith CS, Gubler DJ, .pdf, last accessed 8 July 2013. Roehrig JT, Eaton B, Gould AR, Olson J, Field H, Danials P, Ling AE, Peters CJ, Anderson LJ Chadha MS, Comer JA, Lowe L, Rota PA, Rollin and Mahy BWJ (2000). Nipah virus: A recently PE, Bellini WJ, Ksiazek TG and Mishra A (2006). emergent deadly paramyxovirus. Science 288, 1432­ Nipah virus-associated encephalitis outbreak Siliguri 1435. India. Emerging Infectious Diseases 12, 235-240.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Daniels P, Narasiman M, Gay CG, Roth JA and Middleton DJ, Westbury HA, Morrissy CJ, van Weingartl HM (2008). Hendra and Nipah virus der Heide BM, Russell GM, Braun MA and diseases. Manual of Diagnostic Tests and Vaccinesfor Hyatt AD (2002). Experimental Nipah virus Terrestrial Animals. Chapter 2.9.6. Available at: infection in pigs and cats. Journal of Comparative http://www.oie.int/fileadmin/Home/eng/Health st Pathology 126, 124-136. andards/tahm/2.09.06 HENDRA & NIPAH FIN AL.pdf, last accessed 8 July 2013. OIE (2013). World Animal Health Information Database (WAHID) Interface. Available at: Eaton BT, Broder CC, Middleton D and Wang http://www.oie.int/wahis 2/public/wahid.php/Wah LF (2006). Hendra and Nipah viruses: different and idhome/Home, last accessed 1 July 2103. dangerous. Nature Reviews Microbiology 4, 23-35. Paton NI, Leo YS, Zaki SR, Auchus AP, Lee KE, Epstein JH , Field HE, Luby S, Pulliam JR and Ling AE, Chew SK, Ang B, Rollin PE, Umapathi Daszak P (2006). Nipah virus: impact origins and T, Sng I, Chuan C, Lim E and Ksiazek TG causes of emergence. Current Infectious Disease Reports 8, (1999). Outbreak of Nipah-virus infection among 59-65. abattoir workers in Singapore. Lancet 354, 1253-1256.

Hooper P, Zaki S, Daniels P and Middleton D Tan CT and Wong KT (2003). Nipah encephalitis (2001). Comparative pathology of the diseases caused outbreak in Malaysia. Annals o f the Academy of Medicine by Hendra and Nipah viruses. Microbes and Infection 3, 32, 112-117. 315-322. Wang LF, Collins PL, Fouchier RAM, Kurath G, Katu Y (2004). Nipah virus infection. Uirusu. Journal Lamb RA, Randall RE and Rima BK (2012). of Virology 54, 237-242. Family Paramyxoviridae. In: King AM, Adams MJ, Carstens EB, Lefkowitz EJ (eds.) Virus Taxonomy. Lo MK, Lowe L, Hummel KB, Sazzad HMS, Elsevier, London. Pp. 672-685. Gurley ES, Hossain MJ, Luby SP, Miller DM, Comer JA, Rollin PE, Bellini WJ and Rota PA (2012). Characterization of Nipah virus from outbreaks in Bangladesh, 2008—2010. Emerging Infectious Diseases. Available at: http: / / wwwnc.cdc.gov/ eid / article /18/2/11- 1492 article.htm, last accessed 8 July 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 26. PESTE DES PETITS RUMINANTS VIRUS

26.1. HAZARD IDENTIFICATION 26.1.1. Aetiological agent 26.1.2. Iceland status

Family: Paramyxoviridae; Genus: Morbillivirus; Species: Peste des petits ruminants (PPR) has never been Peste des petits ruminants virus (PPRV) (Lamb et al. reported in Iceland and is listed as a group A 2005). notifiable disease in Act No 25/1993 (Willeberg 2013). Ongoing freedom is supported by general surveillance (OIE 2013).

26.1.3. European Union status

Table 19 (below) summarises the PPR status of the 28 countries of the European Union based on their official returns to the OIE.

Table 19: Status of peste des petits ruminants in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Has never occurred Belgium Freedom Has never occurred Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Has never occurred Germany Freedom Has never occurred Greece Freedom Has never occurred Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom Has never occurred Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Freedom Has never occurred Portugal Freedom Has never occurred Romania Freedom Has never occurred Slovakia Freedom Has never occurred Slovenia Freedom Has never occurred Spain Freedom Has never occurred Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 26.1.4. Epidemiology viraemic period usually precedes the onset of acute clinical signs and high fever. During the acute phase of the disease infected animals excrete virus in ocular Peste des petits ruminants (PPR) occurs in countries and nasal excretions, urine, and faeces (Mushi and in Central, West and North Africa, the Middle East, Wafula 1984; Wafula et al . 1989; Rossiter 2004). Turkey, India, Bangladesh, and China (OIE 2013).

Viraemia begins 1 to 2 days before the onset of illness PPR is a disease mainly of goats and sheep, although and declines when circulating antibody first appears. some species of Bovidae are susceptible, such as nilgai, Animals that recover from PPR do not become gazelles, ibex, and gemsbok (Furley et aL 1987). carriers (Scott 1990). Cattle and pigs are susceptible to infection but do not display clinical signs or transmit infection and are considered to be dead-end hosts (Rossiter 2004; Saliki PPRV may survive for a time in refrigerated meat and and Wohlsein 2008; OIE 2009). There are no reports several months in salted or frozen meat. Lymph of human infection with PPRV (Diallo 2012). nodes from carcasses stored at 4°C contain virus for at least 8 days (Rossiter 2004). Mortality from PPR in sheep and goats varies from 4­ 5% in endemic populations to 20-90% in naïve 26.1.5. Hazard identification conclusion populations (Rossiter 2004). Infection with PPRV occurs most commonly in the oropharynx and upper Although PPRV may persist in meat, the virus has respiratory system through inhalation of aerosol never been recovered from any country in the particles so transmission occurs mainly by close European Union. The geographically limited contact. The incubation period is from 2-6 days distribution of this virus means that it is not (Rossiter 2004). Primary infection establishes in the identified as a hazard in unrestricted meat imports pharyngeal lymph nodes and tonsils and, following a from the European Union. period of viraemia, in all lymphoid tissues. The

References

Diallo A (2012). Chapter 2.7.11. Peste des petits OIE (2013). World Animal Health Information ruminants. In: OIE Manual of Diagnostic Tests and Database (WAHID) Interface. Available at: Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: http://www.oie.int/wahis 2/public/wahid.php/Wah http://www.oie.int/fileadmin/Home/eng/Health st idhome/Home, last accessed 1 July 2103. andards/tahm/2.07.11 PPR.pdf, last accessed 1 July 2013. Rossiter PB (2004). Peste des petits ruminants. In: Coetzer JAW , Tustin RC (eds.) Infectious Diseases of Furley CW, Taylor WP and Obi TU (1987). An Livestock. Oxford University Press, Oxford. Pp. 660­ outbreak of peste des petits ruminants in a zoological 672. collection. Veterinary Record 121, 443-447. Saliki JT and Wohlsein P (2008). Peste des petits Lamb RA, Collins PL, Kolakofsky D, Merelo JA, ruminants. In: United States Animal Health Ngai Y, Oldstone MBA, e t al . (2005). Genus Association (ed.) Foreign Animal Diseases. Boca Morbillivirus. In: Fauquet CM, Mayo MA, Maniloff J, Publications Group, Boca Raton. Pp. 357-364. Desselberger U, Ball LA (eds) Eighth Report o f the International Committee on Taxonomy of Viruses. Elsevier Scott GR (1990). Peste des petits ruminants (goat Academic Press, Amsterdam. Pp. 663-664. plague) virus. In: Dinter Z, Morein B (eds) Virus Infections o f Ruminants. Amsterdam. Pp. 355-375. Mushi EZ and Wafula JS (1984). The shedding of a virulent Kabete O strain of rinderpest virus by cattle. Wafula JS, Rossiter PB, Wamwayi HM and Scott Veterinary Research Communications 8, 173-179. GR (1989). Preliminary observations on rinderpest in pregnant cattle. Veterinary Record 124, 485-486. OIE (2009). Peste des petits ruminants. Technical disease card. Available at: W illeberg P (2013). Chapter 5. Notification and http: / / www.oie.int/fileadmin/Home / eng/Animal animal disease surveillance. In: Risk assessments Health in the World/docs/pdf/PESTE DES PET regarding open trade in live animals to Iceland. Icelandic ITS RUMINANTS FINAL.pdf. last accessed 9 Food and Veterinary Authority (MAST), Reykjavik, August 2013. Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 27. PORCINE EPIDEMIC DIARRHOEA VIRUS

27.1. HAZARD IDENTIFICATION 27.1.1. Aetiological agent In May 2013, a PED virus very similar to the highly virulent strains circulating in Asia was detected in the United States. The virus has been associated with Family: Coronaviridae, Genus: Coronavirus, Species: severe disease outbreaks of PED across the United Porcine epidemic diarrhoea virus (de Groot et al. 2012). States. Infection has been associated with significant losses in preweaning and growing pigs, with 27.1.2. Iceland status morbidity and mortality in affected herds ranging from 30 to 100 per cent (Roberts and Middlemiss Never recorded in Iceland. 2013; United States Department of Agriculture 2013; Williamson et al. 2013). 27.1.3. European Union status PED virus replicates in the cytoplasm of villous epithelial cells throughout the small intestine and Outbreaks of porcine epidemic diarrhoea have been colon, resulting in villous stunting in the small reported in the European Union since it was first intestine. Studies to date have not shown viral reported in England in 1971. replication in cells outside the intestinal tract. PED is primarily thought to be transmitted through the 27.1.4. Epidemiology faecal-oral route by contact with live infected pigs, pig faeces or manure, and contaminated vehicles or Porcine epidemic diarrhoea (PED) was probably first fomites, including feed (Pensaert and Yeo 2006). recognised in England in 1971, but the cause was not established until 1978 when outbreaks were reported The main clinical sign associated with infection is in Belgium and the United Kingdom. Since then profuse watery diarrhoea which may affect all ages. disease has been described throughout much of the Piglets less than 1 to 2 weeks old may die after 3 to 4 world (Pensaert and Yeo 2006). Significant outbreaks days due to dehydration, and an average morality rate of PED were described in Korea in the 1990s that in this age group of 50 per cent is described although subsequently spread across east and south-east Asia. it may be much higher. Most growing pigs recover New PED strains subsequently emerged in China and from infection without treatment unless secondary spread to Vietnam and Thailand. In late 2010, infections occur. Infection in suckling pigs is almost despite vaccination, more than 1 million piglets died uniformly fatal unless the piglets are borne to in China following infection with PEDV with the immune dams (due to prior PED infection) (Pensaert mortality rate in infected piglets reported to be and Yeo 2006). between 80 and 100 percent (Sun et al. 2012). 27.1.5. Hazard identification conclusion

Porcine epidemic diarrhoea is predominantly a disease of very young piglets. The causative virus multiplies only in the cells of the digestive tract and there is no evidence that it is found in pig meat. Therefore, this virus is not identified as a hazard in unrestricted meat imports from the European Union.

References de Groot RJ, Baker SC, Baric R, Enjuanes L et al Pensaert MB and Yeo S-G (2006). Chapter 22: (2012). Genus Alphacoronavirus. In: King AMQ, Porcine epidemic diarrhoea. In: Straw BE, Adams MJ, Carstens EB, Lefkowitz EJ (eds.), Ninth Zimmerman JJ, D'Allaire S, Taylor DJ (eds.), Diseases Report of the International Committee on Taxonomy of o f Swine. 9th edition, Blackwell Publishing, Ames, Viruses. Elsevier Academic Press, Amsterdam. Pp. Iowa. Pp. 367-372. 815-817.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Roberts H and Middlemiss C (2013). Porcine United States Department of Agriculture (2013). epidemic diarrhoea in the USA. Preliminary outbreak Technical note. Porcine epidemic diarrhoea (PED). assessment. Department for Environment, Food and Available at: Rural Affairs, Veterinary & Science Policy Advice, http://www.aphis.usda.gov/animal health/animal d International Disease Monitoring. Available at: is spec/swine/downloads/ped tech note.pdf, last http: / / www.defra.gov.uk/animal-diseases / files / poa- accessed 14 September 2013. ped-20130724.pdf, last accessed 14 September 2013. Williamson S, Strugnell B, Thomson J, Webster Sun RQ, Cai RJ, Chen YQ, Liang PS, Chen DK G, McOrist S, Clarke H and Armstrong D (2013). and Song CX (2012). Outbreak of porcine epidemic Emergence of severe porcine epidemic diarrhoea in diarrhoea in suckling pigs, China. Emerging Infectious pigs in the USA. Veterinary Record 173, 146-148. Disease 18, 161-163.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 28. PORCINE REPRODUCTIVE AND RESPIRATORY SYNDROME VIRUS

28.1. HAZARD IDENTIFICATION 28.1.1. Aetiological agent 28.1.2. Iceland status

Family: Arteriviridae, Genus: Arterivirus, Species: Porcine Porcine reproductive and respiratory syndrome reproductive and respiratory syndrome virus (PRRSV) (PRRS) is listed as a group B notifiable disease in Act (Snijder et al. 2005). No 25/1993 and has never been reported in serological surveys undertaken since 1994 (Willeberg 2013). Ongoing freedom is supported by general and targeted surveillance (OIE 2013).

28.1.3. European Union status

Table 20 (below) summarises the PRRS status of the 28 countries of the European Union based on their official returns to the OIE.

Table 20: Status of porcine reproductive and respiratory syndrome in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Has never occurred Croatia Present No clinical disease Cyprus Present Clinical disease Czech Republic Present No clinical disease Denmark Present Clinical disease Estonia Freedom Last reported December 2011 Finland Freedom Has never occurred France Present Clinical disease G erm any Not reported Greece Freedom Last reported 2001 Hungary Present Restricted to certain zones Ireland Present Clinical disease Italy Freedom Last occurrence unknown Latvia Present No clinical disease Lithuania Freedom Last reported 2007 Luxembourg Freedom Last occurrence unknown Malta Freedom Last reported December 2008 Netherlands Present Clinical disease Poland Not reported Portugal Freedom Last reported June 2006 Romania Freedom Last reported February 2010 Slovakia Freedom Last reported January 2007 Slovenia Present No clinical disease Spain Present Clinical disease Sweden Freedom Last reported 2007 United Kingdom Present Clinical disease

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 28.1.4. Epidemiology days PI the virus was found in diaphragm muscle 24 hours post mortem although by 48 hours post mortem, no virus was detectable in any of the muscle Porcine reproductive and respiratory syndrome was specimens from any of the four pigs held at 4°C. first identified in the United States in 1987 and in Mengeling et al. (1995) isolated PRRSV from meat of Europe in 1990, although PRRSV was not identified only one of six experimentally infected pigs, and until 1991 (Benfield et al. 1992). Retrospective Magar et al. (1995) isolated virus from muscle and serological evidence suggests that PRRSV emerged in lymph nodes of two pigs at 7 days PI but not at 14 North America in the late 1970s (Zimmerman et al. days PI. 2006). During the 1990s PRRSV spread rapidly and has since been reported in most pig-producing countries (Albina 1997). Larochelle and Magar (1997) were unable to isolate PRRSV from 2,190 samples taken from packages of frozen meat from four Canadian processing plants. Transmission of PRRSV has been demonstrated by Similarly, in Chinese Taipei (where 85% of pigs tested multiple routes of exposure: intranasal, intramuscular, at three abattoirs were seropositive for PRRSV), none oral, intrauterine, and vaginal. Pigs are extremely of 472 carcass samples of market pigs at slaughter sensitive to parenteral exposure, but considerably less were positive for virus by RT-PCR (Wang 1999). so by other routes (Zimmerman et al. 2006). These studies collectively demonstrated that the likelihood of isolating virus from meat of pigs at Pigs are the only animals affected by the virus. The slaughter was low and, as a result, it was generally main target cells for PRRSV are macrophages, considered in the 1990s that meat was unlikely to be a particularly those in lungs and lymph nodes. While vehicle for transmission of PRRS (Pharo and Cobb alveolar macrophages are the most favoured cell for 2011). replication, only about 2% of these cells become infected, even at the peak of virus replication in the Van der Linden et al. (2003) demonstrated that, at lungs (European Food Safety Authority 2005). slaughter, meat samples taken from pigs artificially infected with PRRSV were positive by virus isolation. Following infection, there is a rapid onset of viraemia Following freezing and storage for 14 days, some of with replication in a number of organs. Viraemic these samples were able to transmit infection when titres peak within four days of infection. While most fed to naïve recipient pigs, suggesting that there was animals will not be viraemic after 28 days, extended sufficient infectivity in 500 g of raw muscle meat to periods of viraemia of up to nine weeks have been infect recipient pigs. reported (European Food Safety Authority 2005). Shortly after this, Magar and Larochelle (2004) found Viral replication has not been demonstrated in that 19 of 1,027 meat samples (1.85%) randomly muscle or endothelial cells. The presence of virus in collected at two Canadian slaughterhouses were meat is assumed to reflect viraemia (Pharo and Cobb positive for PRRSV by RT-PCR, even though only 2011) although lymphoid tissue could be expected to one sample was positive by virus isolation. When contribute to viral titres in some cuts of meat meat from 11 of the RT-PCR-positive carcasses was (European Food Safety Authority 2005). fed to pairs of recipient pigs, in quantities from 1.05 kg to 1.8 kg over two days, seven of the 11 pairs In endemic areas, most herds become infected (63%) became infected. From this study it may be following the movement of infected pigs or by concluded that approximately 1.2% of pigs at slaughter contaminated semen. Spread from neighbouring can be expected to have infectious virus in meat, at farms can also occur via a range of fomites least under North American conditions, but the titre (Zimmerman et al. 2006), and in high-pig-density of virus will be below the threshold of detection by areas the virus is probably also transmitted through virus isolation (Pharo and Cobb 2011). Although aerosols (Pitkin et al. 2009). both of the above feeding trials exhibited design deficiencies, they both suggest that PRRSV should be However, long-distance spread, most likely by considered a potential hazard in imported pig meat. infected animals and semen, is the major route of transmission, even when local spread is suspected by 28.1.5. Hazard identification conclusion insects or aerosols (Goldberg et al. 2000). PRRS is present in a number of countries in the Several studies carried out in the 1990s reported the European Union and PRRSV has been isolated from isolation of PRRSV from meat and associated pig meat derived from both experimentally infected regional lymph nodes of small numbers of pigs (Farez and commercially slaughtered animals. Reflecting and Morley 1997). Bloemraad et al. (1994) took meat this, PRRSV is identified as a potential hazard in pig samples from four artificially infected pigs, two meat and pig meat products imported from the slaughtered at 5 days post inoculation (PI), and two at European Union. 10 days PI. Virus was present in leg muscle of one pig at 5 days PI. In another pig slaughtered at 10

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 28.2. RISK ASSESSMENT Although quantitative analysis has shown that, 28.2.1. Entry assessment because of the fragility of PRRSV and the effect of post-slaughter processing and handling, there is a negligible likelihood of an infectious dose of PRRSV More than 50% of farms in Europe are infected with being present in muscle tissue after slaughter and PRRSV, although this varies between regions; with processing, the presence of lymph nodes in imported lower prevalence seen in areas of low pig density such meat poses a much greater risk (Pharo and Cobb as France and Great Britain (Albina 1997). Given 2011). that the seroprevalence within an affected farm can reach 85-95% within 3 months after the introduction The proportion of lymphoid tissue in fresh meat of infection and this may be followed by a prolonged cannot be quantified. Visible lymph nodes can be persistence of infection (Albina, 1997), it is likely that removed during the trimming process but this is done pigs will be exposed to PRRSV infection prior to slaughter. Given the age at which a pig is likely to not necessarily and not systematically. Lymph nodes in locations not accessible during slaughter (within become infected with PRRSV, the presence and duration of viral infection/contamination in pig meat groups of muscles or viscera) will not be removed and the age at which pigs are slaughtered, Pharo (European Food Safety Authority 2005). It has been estimated that a 20g lymph node taken from a pig (2006) concluded that there was a low likelihood of slaughtered in a country where PRRS is present has a virus being present in the meat of pigs at slaughter. 0.26% likelihood of containing an infectious dose of This conclusion is consistent with the results of empirical studies described above by Van der Linden PRRSV (Pharo and Cobb 2006). If unrestricted import of fresh pig meat from the European Union et al. (2003) and Magar and Larochelle (2004). were permitted, there is a non-negligible likelihood that sufficient virus may be present in associated The likelihood of viable PRRSV being present in pigs lymph nodes (especially those of the head and neck) at slaughter has been the subject of detailed reviews and lymphoid tissues to constitute an infectious dose by the European Food Safety Authority, the New if fed to a naïve pig in Iceland. Zealand government, and the Australian government (Department of Agriculture, Fisheries and Forestry There is a non-negligible likelihood of pigs in Iceland 2004; European Food Safety Authority 2005; Pharo being exposed to PRRSV from unrestricted imports 2006). All three of these comprehensive reviews of pig meat from countries where PRRS is present. concluded that there was a low likelihood that fresh pig meat from a country with PRRS would contain viable PRRSV. 28.2.3. Consequence assessment

The likelihood of PRRSV being present in imported If PRRSV were introduced into a small hobby herd pig meat is assessed to be non-negligible. of pigs, it is likely that there would be few clinical signs, and it is unlikely that an incursion would be 28.2.2. Exposure assessment detected in such an infected herd. The consequences would be limited to that establishment itself, unless there were movement of infected animals, genetic Although there are a small number of commercial pig material, or fomites to other herds (Pharo 2006). farms in Iceland, there has been an increase in the number of people keeping a small number of pigs as a ‘hobby’. In addition there has been an increase in The increasing trend in keeping small herds of pigs in Iceland has been largely driven by the domestic the number of sheep or cattle farms that keep a small herd of pigs. Although it is unlikely that commercial industry’s desire to increase the visibility of this pig farms in Iceland would use kitchen waste as a species in Iceland and raise consumer awareness of source of feed, it is highly likely that kitchen waste food production. It would therefore be reasonable to conclude that there is more connectivity between would be used as an inexpensive source of feed for these hobby herds and the commercial industry in pigs in small hobby herds. Iceland than may be seen in other countries.

PRRSV is completely inactivated in tissue cultures Although the movement of infected pigs is likely to containing a starting titre of 105 TCID 50 per 100 gl by holding them for 45 minutes at 56°C (Benfield et al. be the major route of spread between herds in 1992), and a 3 log decline in virus titre is seen after countries where PRRS is present, a wide range of one hour at 56°C (Bloemraad et al. 1994). PRRSV is fomites (boots, clothing, hands, equipment, vehicles) therefore very sensitive to thermal inactivation so any have been suggested to transmit infection between scraps of cooked pig meat are unlikely to contain herds (Benfield et al, 1999). Contaminated boots, clothing, and hypodermic needles have been shown viable virus. However, viable virus is likely to remain to transmit infection (Otake et al. 2002a; Otake et al. in any raw (uncooked) meat waste generated prior to cooking. 2002b). Although this mechanical transmission via fomites can be expected during warm weather (Dee et al. 2002b), it is more likely to be seen during winter

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union when the virus might be expected to survive for reduction in expected profits for the year of the longer periods in the environment (Dee et al. 2002a). outbreak), with projected total costs over a 3 year Reflecting the connectivity between Iceland’s period of around US$500 per sow (Polson et al domestic pig industry and the growing number of 1990). small hobby herds, and the possible routes of transmission of infection between these, there is a The consequences of introduction as therefore non-negligible likelihood that infection of a small assessed to be non-negligible. hobby herd would spread to Iceland’s commercial industry. 28.2.4. Risk estimation The major production losses associated with the introduction of PRRSV into a commercial pig farm Since entry, exposure, and consequence assessments are likely to be as a result of a large reduction in are non-negligible, the risk estimation is non- farrowing rate. This was estimated (in 1990) to negligible and PRRSV is assessed to be a risk in amount to US$236 per sow (equivalent to an 80% unrestricted pig meat imports from the European Union. References

Albina E (1997). Epidemiology of porcine Dee S, Deen J, Rossow K, Wiese C, Eliason R, reproductive and respiratory syndrome (PRRS): an Otake S, Joo HS and Pijoan C (2002b). overview. Veterinary Microbiology 55, 309-316. Mechanical transmission of porcine reproductive and respiratory syndrome virus throughout a coordinated Benfield DA, Nelson E, Collins JE, Harris L, sequence of events during warm weather. Canadian Goyal SM, Robinson D, Christianson WT, Journal of Veterinary Research 67, 12-19. Morrison RB, Gorcyga DE and Chladek DW (1992). Characterization of swine infertility and European Food Safety Authority (EFSA) (2005). respiratory syndrome (SIRS) virus (isolate ATCC- The probability of transmission of porcine VR2332). Journal o f Veterinary Diagnostic Investigation 4, reproductive and respiratory syndrome virus (PRRSv) 127-133. to naïve pigs via fresh meat. EFSA Journal 239, 1-85.

Benfield DA, Collins JE, Dee SA, Halbur PG, Joo Farez S and Morley RS (1997). Potential animal HS, Lager KM, Mengeling WL, Murtaugh MP, health hazards of pork and pork products. In Rossow KD, Stevenson GW and Zimmerman JJ Contamination of animal products: prevention and (1999). Porcine Reproductive and Respiratory Syndrome. In: risks for animal health (P. Sutmoller, ed.). Revue Straw ES, D’Allaire S, Mengeling WL, Taylor DJ Scientifique et Technique Office International des Épizooties (eds). Disease of Swine (8th edition). Iowa State 16, 65-78. University Press, Ames. Pp. 201-232. Goldberg TL, Hahn EC, Ronald M, Weigel RM Bloemraad M, de Kluijver EP, Petersen A, and Scherba G (2000). Genetic, geographical and Burkhardt G and Wensvoort G (1994). Porcine temporal variation of porcine reproductive and reproductive and respiratory syndrome: temperature respiratory syndrome virus in Illinois. Journal of and pH stability of Lelystad virus and its survival in General Virology 81, 171-179. tissue specimens from viraemic pigs. Veterinary Microbiology 42, 361-371. Larochelle R and M agar R (1997). Evaluation of the presence of porcine reproductive and respiratory Department of Agriculture, Fisheries and syndrome virus in packaged pig meat using virus Forestry (2004). Generic import risk analysis (IRA) isolation and polymerase chain reaction (PCR) for pig meat. Final import risk analysis report. method. Veterinary Microbiology 58, 1-8. Available at: http://www.daff.gov.au/ data/assets/pdf file/001 M agar R and Larochelle R (2004). Evaluation of 8/18081/2004-01b.pdf, last accessed 24 September the presence of porcine reproductive and respiratory 2014. syndrome virus in pig meat and experimental transmission following oral exposure. Canadian Journal Dee S, Deen J, Rossow K, Wiese C, Otake S, Joo of Veterinary Research 68, 259-266. HS and Pijoan C (2002a). Mechanical transmission of porcine reproductive and respiratory syndrome Magar R, Robinson Y, Dubuc C and Larochelle virus throughout a coordinated sequence of events R (1995). Evaluation of the persistence of porcine during cold weather. Canadian Journal o f Veterinary reproductive and respiratory virus in pig carcasses. Research 66, 232-239. Veterinary Record 137, 559-561.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Mengeling WL, Lager KM and Vorwald AC Polson DD, Marsh WE and Dial GD (1990). (1995). Diagnosis of porcine reproductive and Financial implications of mystery swine disease. respiratory syndrome. Journal of Veterinary Diagnostic Proceedings o f Mystery swine disease Meeting. Livestock Investigation 7, 3-16. Convention Institute Denver, 1990. Pp. 8-28.

OIE (2013). World Animal Health Information Snijder EJ, Brinton MA, Faaberg KS, Godeny Database (WAHID) Interface. Available at: EK, E. GA, MacLachlan NJ, Mengeling WL and http: / /www.oie.int/wahis 2/public/wahid.php/Wah Plageman PGW (2005). Genus Arterivirus. In: idhome/Home, last accessed 1 July 2103. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds), Eighth Report o f the International Committee Otake S, Dee SA, Rossow KD, Joo HS, Deen J, on Taxonomy of Viruses. Elsevier Academic Press, Molitor TW and Pijoan C (2002a). Transmission of Amsterdam. Pp. 965-974. porcine reproductive and respiratory syndrome virus by needles. Veterinary Record 150, 114-115. Van der Linden IFA, van der Linde-Bril EM, Voermans JJM , van Rijn PA, Pol JMA, Martin R Otake S, Dee SA, Rossow KD, Deen J, Joo HS, and Steverink PJGM (2003). Oral transmission of Molitor TW and Pijoan C (2002b). Transmission porcine reproductive and respiratory syndrome virus of porcine reproductive and respiratory syndrome by muscle of experimentally infected pigs. Veterinary virus by fomites (boots and coveralls). Journal of Swine Microbiology 97, 45-54. Health and Production 10, 59-65. W ang FI (1999). Minimal residues of porcine Pharo (2006). Import risk analysis: Porcine reproductive and respiratory syndrome virus in pig reproductive and respiratory syndrome (PRRS) virus carcases and boar semen. Proceedings of the National in pig meat. Biosecurity New Zealand, Wellington, Science Council, Republic of China. Part B 23, 167-174. New Zealand. Available at: http: / / www.biosecurity.govt.nz / files / regs / imports / r W illeberg P (2013). Chapter 5. Notification and isk/prrs-risk-analysis.pdf, last accessed 24 September animal disease surveillance. In: Risk assessments 2013. regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Pharo HP and Cobb SP (2011). The spread of Iceland. Pp. 59-90. pathogens through trade in pig meat: overview and recent developments. In Disease transmission Zimmerman J, Benfield DA, Murtaugh MP, through international trade (MacDiarmid S, ed.). Osoria F, Stevenson GW and Torremorell M Revue Scientifique et Technique Office International des (2006). Porcine reproductive and respiratory Épigooties 30, 139-148. syndrome virus (porcine arterivirus). In Diseases of swine (BE Straw, JJ Zimmerman, S D’Allaire and DJ Pitkin AN, Deen J and Dee SA (2009). Use of a Taylor, eds), 9th Ed. Blackwell Publishing, Iowa. Pp. production region model to assess the airborne 387-417. spread of porcine reproductive and respiratory syndrome virus. Veterinary Microbiology 136, 1-7.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 29. PORCINE TESCHOVIRUS

29.1. HAZARD IDENTIFICATION 29.1.1. Aetiological agent 29.1.2. Iceland status

Family: Picornaviridae, Genus: Teschovirus. Eleven Teschovirus encephalomyelitis has never been serotypes of porcine Teschovirus (PTV) are described in Iceland. recognised, PTV-1 to PTV-11. Virulent strains of PTV-1 are associated with Teschovirus encephalitis (Teschen disease) whereas less virulent strains of 29.1.3. European Union status PTV-1 are associated with milder disease (Talfan disease, benign enzootic paresis, or poliomyelitis Until 2010, teschovirus encephalomyelitis was an suum) (Zell et al. 2001; Center for Food Security and OIE-Listed disease. The previously reported status Public Health 2009). of European Union members is shown below in table 21.

Table 21: Status of teschovirus encephalomyelitis in European Union countries based on their historical (2005) returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported 1980 Belgium Freedom Has never occurred Bulgaria Freedom Has never occurred Croatia Freedom Last reported 1956 Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 1973 Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Has never occurred Germany Freedom Last reported 1957 Greece Freedom Has never occurred Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom Has never occurred Latvia Freedom Last reported 2002 Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Freedom Last reported 1967 Portugal Freedom Has never occurred Romania Freedom Last reported 2002 Slovakia Freedom Last reported 1973 Slovenia Freedom Has never occurred Spain Freedom Has never occurred Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

29.1.4. Epidemiology Teschovirus encephalomyelitis. Teschen disease (a fatal, nonsuppurative encephalomyelitis of pigs) was first described in the Czech Republic in 1929 and Most of the eleven serotypes of PTV are widely later spread throughout Europe (Knowles 2008). A distributed in pigs and cause few clinical problems. milder form of disease (Talfan disease or However, virulent strains of PTV-1 cause poliomyelitis suum) was later described in Wales and

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Denmark (Yamada et aL 2009). Clinical signs of et aL 2009). Histological studies on field outbreaks of infection with virulent strains of PTV-1 include disease suggest pathological lesions are limited to the fever, anorexia, depression and incoordination brain and spinal cord (Pogranichniy et aL 2003). PTV followed by hypersensitivity, paralysis and death. infections only occur in swine. Other animal species Less virulent strains of PTV-1 (and strains of PTV-2, are not known to be susceptible (Knowles 2008). PTV-3, PTV-4, PTV-5, PTV-6, PTV-9, and PTV-10) are associated with neurological disease in younger The disease is now considered to be rare since there animals characterised by ataxia and paresis which may have been no outbreaks recorded worldwide for a progress to paralysis (Knowles 2008; Center for Food number of years (Knowles 2008; Emergency Security and Public Health 2009). Prevention System 2009). However, historically outbreaks of Teschen disease have been attributed to Natural infection of pigs by enteroviruses is by the imported meat products (Scientific Veterinary oral route. The virus replicates in the intestines and a Committee 1997). transient viraemia may last several days. Dependent on the infecting strain, disease may go unnoticed, or 29.1.5. Hazard identification conclusion cause polioencephalomyelitis and paralysis. The infected pig excretes large amounts of virus in the faeces, contaminating the environment. The faecal- The main route of transmission of PTV-1 is faecal- oral route is the most important means of oral, directly or indirectly from contaminated sources transmission (Alexander 2004; Center for Food of food or water and there is very little evidence Security and Public Health 2009). suggesting contaminated meat could act as a source of infection. Following experimental intravenous infection with PTV-1, viral antigen was detected in spinal ganglia, Although PTV-1 strains are present in pigs degenerate nerve fibres, brainstem grey matter, and worldwide, virulent strains of PTV-1 causing ventral horn of the spinal cord as well as in teschovirus encephalomyelitis are now rare and there bronchiolar epithelial cells, hepatocytes, tonsillar is no evidence that these viruses are present in the epithelium and myenteric nerve plexus of the small European Union. and large intestine. Viral antigen was only seen in the enterocytes of the duodenum and jejunum and in the Porcine teschoviruses are not identified as a hazard in tonsils following oral infection with PTV-1 (Yamada unrestricted meat imports from the European Union.

References

Alexander TJL (2004). Teschen, Talfan and Knowles N (2008). Chapter 2.8.10. Teschovirus reproductive diseases caused by porcine encephalomyelitis (previously enterovirus enteroviruses. In: Coetzer JAW , Tustin RC (eds.) encephalomyelitis or Teschen/Talfan disease). In: Infectious Diseases o f Livestock. Oxford University Press, Manual o f Diagnostic Tests and Vaccines fo r Terrestrial Cape Town. Pp. 1307-1309. Animals. OIE, Paris. Available at: http://www.oie.int/fileadmin/Home/eng/Health st Center for Food Security and Public Health andards /tahm/2.08.10 TESCHOVIRUS ENCEPH. (2009). Teschovirus encephalomyelitis and porcine pdf, last accessed 14 September 2013. Teschovirus infection. Available at: http: / / www.cfsph.iastate.edu /Factsheets / pdfs/ enter OIE (2013). World Animal Health Information ovirus encephalomyelitis.pdf , last accessed 14 Database (WAHID) Interface. Available at: September 2013. http://www.oie.int/wahis 2/public/wahid.php/Wah idhome/Home, last accessed 14 September 2103. Emergency Prevention System (2009). Teschovirus encephalomyelitis in the Republic of Pogranichniy RM, Janke BH, Gillespie TG and Haiti. Food and Agriculture Organization of the Yoon K-J (2003). A prolonged outbreak of United Nations. Available at: polioencephalomyelitis due to infection with a group http: / / www.oirsa.org/aplicaciones / subidoarchivos / I porcine enterovirus. Journal of Veterinary Diagnostic BibliotecaVirtual/Focus ON Teschovirus en.pdf Investigation 15, 191-194. last accessed 14 September 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Scientific Veterinary Committee (1997). The Yamada M, Kozakura R, Nakamura K, Assessment of Risk from “Sibiu Salami” coming Yamamoto Y, Yoshii M, Kaku Y, Miyazaki A, from Classical Swine Fever, Swine Vesicular Disease Tsunemitsu H and Narita M (2009). Pathological and Teschen Disease Potentially Infected Areas. changes in pigs experimentally infected with porcine Available at: Teschovirus. Journal of Comparative Pathology 141, 223­ http: //ec.europa.eu/food/fs/sc/oldcomm4/out26 e 228. n.pdf, last accessed 14 September 2013. Zell R, Dauber M, Krumbholz A, Henke A, Birch-Hirschfeld E, Stelzner A, Prager D and Wurm R (2001). Porcine Teschoviruses comprise at least eleven distinct serotypes: Molecular and evolutionary aspects. Journal of Virology 75, 1620-1631

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 30. SWINE VESICULAR DISEASE VIRUS

30.1. HAZARD IDENTIFICATION 30.1.1. Aetiological agent 30.1.2. Iceland status

Family: Picornaviridae, Genus: Enterovirus, Species: Swine vesicular disease (SVD) has never been Swine vesicular disease virus (SVDV). SVDV is reported in Iceland and is listed as a group A considered to be a porcine variant of Human notifiable disease in Act No 25/1993 (Willeberg coxsackievirus B5 (Stanway et al. 2005). 2013). Ongoing freedom is supported by general surveillance (OIE 2013).

30.1.3. European Union status

Table 22 (below) summarises the SVD status of the 28 countries of the European Union based on their official returns to the OIE.

Table 22: Status of swine vesicular disease in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported January 1979 Belgium Freedom Last reported February 1993 Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Last reported 1983 Germany Freedom Last reported 1985 Greece Freedom Last reported 1979 Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom ? Last reported June 2012 Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Last reported 1979 Netherlands Freedom Last reported February 1994 Poland Freedom Last reported 1972 Portugal Freedom Last reported June 2007 Romania Freedom Last reported 1985 Slovakia Freedom Has never occurred Slovenia Freedom Has never occurred Spain Freedom Last reported April 1993 Sweden Freedom Has never occurred United Kingdom Freedom Last reported 1982

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 30.1.4. Epidemiology

Swine vesicular disease (SVD) first emerged in Italy SVDV is resistant to a wide range of pH including in 1966 (Nardelli et al. 1968) and was subsequently low pH conditions, remaining viable in meat after seen throughout other parts of Europe and in Asia rigor mortis (pH<6.0). The virus is resistant to (Lubroth et al. 2006). Currently SVD is seen salting and smoking processes, survives desiccation, sporadically in southern and central Italy (OIE 2009; and may remain in dry-cured hams for 180 days, OIE 2013). dried sausages for over 1 year, and in processed intestinal casings for over 2 years (Center for Food Safety and Public Health 2007; Torres 2008; OIE SVDV is highly contagious by direct contact with 2009). infected animals or from a contaminated environment (Dekker et al. 1995). The virus can survive for more than one month outside the host 30.1.5. Hazard identification conclusion and significant transmission via fomites or waste feeding can occur (Hedger and Mann 1989; Torres SVD is sporadically reported in Italy although all 2008). Infected pigs excrete virus up to 48 hours other countries in the European Union report before the onset of clinical signs. Virus is generally freedom from this disease. Pig meat is recognised as eliminated within two weeks of infection, but in rare a vehicle for the introduction of this disease so cases infection may persist for up to three months SVDV is identified as a potential hazard in pig meat with the virus excreted in the faeces (OIE 2009). and pig meat products imported from the European Union. Disease is transient and it is not life threatening. The key significance of SVD is that it strongly resembles 30.2. RISK ASSESSMENT other vesicular diseases, particularly foot and mouth disease (Center for Food Safety and Public Health 30.2.1. Entry assessment 2007; OIE 2009). Pigs may be viraemic before the onset of clinical Clinical signs are characterised by the formation of signs. Recently infected animals may not be detected vesicles and erosions around the coronary bands, at ante-mortem and post-mortem inspection. interdigital spaces and on the skin of the lower legs, Animals that are presented at slaughter in the particularly at pressure points such as the stifles. incubation phase of infection are likely to have Vesicles are occasionally seen on the snout, lips, contaminated meat products produced from them. tongue, and teats. The vesicles rupture leaving Recent outbreaks of SVD have been characterised by shallow erosions. When pigs are kept on abrasive less severe or no clinical signs, which increases the flooring or in wet and unsanitary conditions, clinical likelihood of infected animals going undetected when signs are more severe. Conversely, pigs kept on grass presented for slaughter (OIE 2009). or housed on deep straw may show little or no noticeable clinical signs (OIE 2009). All porcine tissues contain virus during the viraemic period and SVDV is likely to survive for prolonged Viral titres are greatest in the myocardium and brain periods in meat and meat products (OIE 2009). of infected individuals, suggesting these are the most Therefore, the likelihood of entry of SVDV in pig likely sites of viral replication (Chu et al. 1979; Lai et meat imported from the European Union is assessed al. 1979). Experimental inoculation studies have to be non-negligible. demonstrated high viral titres in lymph nodes (Dekker et al. 1995). All porcine tissues are thought 30.2.2. Exposure assessment to contain virus during the viraemic period (OIE 2009). Such tissues can transmit infections if Should contaminated meat products harbouring undercooked pork meat or other scraps are fed to SVDV be imported, the only plausible route of swine. The disease has been introduced into new exposure would be from subsequent feeding to pigs. herds by the feeding of infected swill containing meat Although there are a small number of commercial pig scraps from infected swine (Torres 2008). All tissues farms in Iceland, there has been an increase in the of infected pigs contain the SVD virus and can serve number of people keeping a small number of pigs as as vehicles for transmission of infection. a ‘hobby’. In addition there has been an increase in International transport of infected meat is probably the number of sheep or cattle farms that keep a small the main route by which SVD virus spread around herd of pigs. Although it is unlikely that commercial the world in the 1960s (MacDiarmid 1991). pig farms in Iceland would use kitchen waste as a source of feed, it is highly likely that kitchen waste would be used as an inexpensive source of feed for pigs in small hobby herds.

The likelihood of exposure is assessed to be low.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 30.2.3. Consequence assessment If SVDV established in Iceland’s commercial pig population, a high incidence of infection but with a very low mortality could be expected. Further, low Clinical signs of SVD resemble other vesicular morbidity and negligible production losses would diseases, particularly foot and mouth disease. Since probably result (European Food Safety Authority clinical signs are indistinguishable from those caused 2012). Therefore, the significance and impact of by foot and mouth disease and vesicular stomatitis, SVD is considered to be low. an outbreak of SVD would prompt an immediate response and require laboratory diagnostics to differentiate the possible causes. A confirmed SVDV infects pigs only. There would be no incursion of SVD would likely result in a response to consequences for any other animals and there is no eradicate the disease, most likely including significant human health threat. culling and disposal. The consequences are assessed to be low. The increasing trend in keeping small herds of pigs in Iceland has been largely driven by the domestic 30.2.4. Risk estimation industry’s desire to increase the visibility of this species in Iceland and raise consumer awareness of Since entry, exposure, and consequence assessments food production. It would therefore be reasonable to are non-negligible, the risk estimation is non- conclude that there is more connectivity between negligible and SVDV is assessed to be a risk in these hobby herds and the commercial industry in unrestricted pig meat imports from the European Iceland than may be seen in other countries. Union. Therefore, the introduction of SVD into a small hobby herd in Iceland would be likely to result in infection being introduced into the commercial sector. References

Center for Food Safety and Public Health (2007). Lubroth J, Rodríguez L and Dekker A (2006). Swine vesicular disease. The Center fo r Food Security and Vesicular diseases. In: Straw BE, Zimmerman JJ, Public Health. Available at: D’Allaire S, Taylor DJ (eds) Diseases o f Swine 9th http://www.cfsph.iastate.edu/Factsheets/pdfs/swine Edition. Blackwell Publishing. Pp. 517-535. vesicular disease.pdf, last accessed 11 August 2013. MacDiarmid SC (1991). The importation into New Chu RM, Moore DM and Conroy JD (1979). Zealand of meat and meat products. A review of the Experimental swine vesicular disease, pathology and risks to animal health. Ministry of Agriculture and immunofluorescence studies. Canadian Journal of Fisheries New Zealand, Wellington, New Zealand. Comparative Medicine 43, 29-38. Available at: http: / / www.biosecurity.govt.nz / files / regs / imports / r Dekker A, Moonen P, de Boer-Luijtze EA and isk/meat-meat-products-ra.pdf last accessed 2 Terpstra C (1995). Pathogenesis of swine vesicular September 2013. disease after exposure of pigs to an infected environment. Veterinary Microbiology 45, 234-250. Nardelli L, Lodetti E, Gualandi GL, Burrows R, Goodridge D, Brown F and Cartwright B (1968). European Food Safety Authority (2012). Scientific A foot and mouth disease syndrome in pigs caused opinion on swine vesicular diseases and vesicular by an enterovirus. Nature 219, 1275-1276. stomatitis. European Food Safety Authority Journal, 10 (4), 2631. Available at: OIE (2009). Swine Vesicular Disease. Technical disease http: / / www.efsa.europa.eu/en/efsajournal/pub/263 card. Available at: 1.htm, last accessed 25 September 2013. http: / / www.oie.int/fileadmin/Home/eng/Animal Health in the World/docs/pdf/SWINE VESICU Hedger RS and Mann JA (1989). Swine vesicular LAR DISEASE FINAL.pdf , last accessed 11 disease virus. In Pensaert MB (ed) Virus Infections o f August 2013. Vertebrates, Volume 2. Virus Infections o f Porcines. Elsevier Science Publishers. Pp. 241-250, OIE (2013). World Animal Health Information Database (WAHID) Interface. Available at: Lai SS, McKercher PD, Moore DM and Gillespie http://www.oie.int/wahis 2/public/wahid.php/Wah JH (1979). Pathogenesis of swine vesicular disease in idhome/Home, last accessed 1 July 2103. pigs. American Journal of Veterinary Research 40, 463­ 468.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Stanway G, Brown F, Christian P, Hovi T, Torres A (2008). Swine vesicular disease. In: United Hyypia T, King AMQ, Knowles NJ, Lemon SM, States Animal Health Association (ed.) Foreign Animal Minor PD, Pallansch MA and Palmenberg AC Diseases. Boca Publications Group, Boca Raton. Pp. (2005). Genus Enterovirus. In: Fauquet CM, Mayo 397-400. MA, Maniloff J, Desselberger U, Ball LA (eds), Eighth Report of the International Committee on Taxonomy of W illeberg P (2013). Chapter 5. Notification and Viruses. Elsevier Academic Press, Amsterdam. Pp. animal disease surveillance. In: Risk assessments 760-763. regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 31. TRANSMISSIBLE GASTROENTERITIS VIRUS

31.1. HAZARD IDENTIFICATION 31.1.1. Aetiological agent 31.1.3. European Union status

Family: Coronaviridae, Genus: Coronavirus, Species: Table 23 (below) summarises the TGE status of the Transmissible gastroenteritis virus (TGEV) (Spaan et al. 28 countries of the European Union based on their 2005). official returns to the OIE.

31.1.2. Iceland status

Transmissible gastroenteritis (TGE) has never been reported in Iceland and is listed as a group A notifiable disease in Act No 25/1993. Surveys undertaken in 1994, 1998, and 2007 returned no positive results (Willeberg 2013). Ongoing freedom is supported by general and targeted surveillance (OIE 2013).

Table 23: Status of transmissible gastroenteritis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last reported 2004 Bulgaria Freedom Last reported 1997 Croatia Freedom Last reported 2004 Cyprus Freedom Last reported June 2011 Czech Republic Freedom Last reported 1998 Denmark Freedom Has never occurred Estonia Freedom Last reported 1986 Finland Freedom Last reported 1980 France Not reported Germany Freedom Last reported February 2012 Greece Freedom Last occurrence unknown Hungary Freedom Last reported 1968 Ireland Freedom Last reported 1984 Italy Freedom Last occurrence unknown Latvia Freedom Last reported March 1985 Lithuania Freedom Last reported 1990 Luxembourg Freedom Last occurrence unknown Malta Freedom Last reported 2001 Netherlands Freedom Last occurrence unknown Poland Freedom Last reported 1997 Portugal Freedom Last reported 1996 Romania Freedom Last reported 2004 Slovakia Freedom Last occurrence unknown Slovenia Freedom Last occurrence unknown Spain Freedom Last reported June 2012 Sweden Freedom Has never occurred United Kingdom Freedom Last reported 1999

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 31.1.4. Epidemiology TGEV was not recovered from blood, pharyngeal swab, muscle, lymph node, or bone marrow samples from acutely infected six-month-old pigs although Transmissible gastroenteritis causes high mortality in homogenates of these tissues, when fed to three- neonatal pigs. It occurs in North America and has week-old piglets (1.5 kg each over five days) resulted previously been described in many European in a serological response. However, no clinical signs countries (OIE 2013). Since the emergence and rapid of infection were seen in these piglets suggesting that spread throughout Europe of porcine respiratory TGEV may have been present in carcass tissues at a coronavirus (PRCV), a large proportion of the pig very low level, below the level detectable by virus population has acquired immunity to PRCV, and isolation (Forman 1991). consequently, also to TGEV. The endemicity of PRCV has thus markedly decreased the clinical and economic importance of TGE (Pensaert and Van TGEV was isolated from four of 500 tonsil samples Reeth 2004). taken from commercially slaughtered pigs although virus was not isolated from pooled muscle and lymph node homogenates. Feeding two groups of ten When introduced into a naïve herd TGEV infects all neonatal piglets five millilitres of the homogenate ages; pigs under 7 days invariably die, suckling pigs daily for four days caused five deaths and older than 7 days usually survive but remain stunted, seroconversion in the survivors although the housing and older animals generally show inappetance and of the two groups may have allowed horizontal diarrhoea for a few days before recovering (Saif and transmission to occur. Despite this, the authors of Sestak 2006). Lactating sows may become very sick this study concluded that at least one homogenate fed with signs of inappetance, vomiting, diarrhoea, and to each group contained virus and that carcass tissue agalactia (Saif and Sestak 2006). Cats and dogs can of at least two of the 500 slaughtered pigs had be subclinically infected (Pensaert and Van Reeth contained viable TGE virus (Cook et al. 1991). 2004).

A more recent review of the potential animal health Pigs commonly carry TGEV for 2 weeks after hazards associated with the importation of pork and infection (Pensaert and Van Reeth 2004), although pork products (Farez and Morley 1997) assessed chronic shedding of the virus for periods up to 18 these experiments carried out by Forman (1991) and months has been reported (Derbyshire et al. 1969). Cook et al. (1991) and concluded that viral titres in After an outbreak of the disease some herds eliminate muscle tissues of slaughter age pigs do not exist since the virus, but in larger herds with frequent farrowings a viraemic phase of TGE does not occur in this age the virus may become endemic (Saif and Sestak of pigs. For this reason, TGEV was not a hazard 2006). associated with imported pork and pork products.

Transmission is usually by the faecal-oral route when susceptible pigs come in contact with infected pigs or 31.1.5. Hazard identification conclusion when faeces are carried on fomites (Saif and Sestak 2006). The primary site of replication is in the small Although there may be some uncertainty regarding intestine and the virus is shed in large quantities with the likelihood that pig meat may act as a vehicle for faeces. Transmission is by the faecal-oral route when the introduction of TGE, this disease is not susceptible pigs come in contact with infected pigs or recognised in the European Union so TGEV is not when faeces are carried on fomites (Saif and Sestak identified as a hazard in unrestricted meat imports 2006). from the European Union.

References

Cook DR, Hill HT and Taylor JD (1991). Oral Farez S and Morley RS (1997). Potential animal transmission of transmissible gastroenteritis virus by health hazards of pork and pork products. Review muscle and lymph node from slaughtered pigs. Scientifique et Technique de l'Office International des Australian Veterinary Journal 68, 68-70 Epizooties 16, 65-78.

Derbyshire JB, Jessett DM and Newman G Forman AJ (1991). Infection of pigs with (1969). An experimental epidemiological study of transmissible gastroenteritis virus from contaminated porcine transmissible gastroenteritis. Journal o f carcases. Australian Veterinary Journal 68, 25-27. Comparative Pathology 79, 445-452.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union OIE (2013). World Animal Health Information Spaan WJM, Brian D, Cavanagh D, de Groot R, Database (WAHID) Interface. Available at: J., Enjuanes L, Gorbalenya AE, Holmes KV, http: / /www.oie.int/wahis 2/public/wahid.php/Wah Masters P, Rottier P, Taguchi F and Talbot P idhome/Home, last accessed 1 July 2103. (2005). Genus Coronavirus. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds), Eighth Pensaert MB and Van Reeth K (2004). Report o f the International Committee on Taxonomy of Transmissible gastroenteritis. In: Coetzer JAW, Viruses. Elsevier Academic Press, Amsterdam. Pp. Tustin RC (eds), Infectious Diseases of Livestock. Oxford 947-955. University Press, Cape Town. Pp. 780-783. W illeberg P (2013). Chapter 5. Notification and Saif LJ and Sestak K (2006). Transmissible animal disease surveillance. In: Risk assessments gastroenteritis and porcine respiratory coronavirus. regarding open trade in live animals to Iceland. Icelandic In: Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ Food and Veterinary Authority (MAST), Reykjavik, (eds), Diseases o f Swine. 9th edition, Blackwell Iceland. Pp. 59-90. Publishing, Ames, Iowa. Pp. 489-516.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 32. VESICULAR EXANTHEMA OF SWINE VIRUS

32.1. HAZARD IDENTIFICATION 32.1.1. Aetiological agent Vesicular exanthema is clinically indistinguishable from either foot and mouth disease or vesicular stomatitis. Infected pigs present with vesicles on the Family: Caliciviridae, Genus: Vesivirus. Vesicular snout, lips, tongue, and mucosae of the oral cavity exanthema of swine virus (VESV) and vesiviruses and on the sole, interdigital spaces, and coronary isolated from marine species are grouped together as band of the foot. Lesions directly attributable to “marine vesiviruses” (King et al. 2012). VESV, other than vesicle formation, have not been described (Madin and Traum 1955). 32.1.2. Iceland status VES most likely originated from pigs eating infected One outbreak of vesicular exanthema of swine (VES) marine mammals or fish tissues since the virus is has been described historically in Iceland more than stable in meat products even when decomposed. 50 years ago. VESV is principally transmitted between pigs by direct contact when ruptured vesicles release large 32.1.3. European Union status amounts of infective virus into the environment (Madin and Traum 1955; Knowles 2004; Torres 2008). This disease has never been reported in the European Union. The only outbreak of this disease reported outside the United States was in Iceland. 32.1.5. Hazard identification conclusion

32.1.4. Epidemiology Vesicular exanthema is a historical disease that has not been reported since 1956. Furthermore, VES has never been reported in the European Union. VESV The primary reservoir hosts of marine vesiviruses are is not identified as a hazard in unrestricted meat thought to be certain fish species (especially the imports from the European Union. opaleye fish (Girella nigricans)) which can pass on infections to secondary hosts such as marine mammals (certain species of sea lions, seals, and dolphins) or pigs. VES was first reported in pigs in the United States in 1932 and outbreaks continued until it was eradicated in 1956. Only one outbreak has been described outside of the United States (in Iceland, associated with pigs fed raw garbage from a United States military post). In domestic animals, VES is a disease of pigs only (Anon 1988; Knowles 2004; Torres 2008; Iowa State University 2011).

References

Anon (1988). Vesicular exanthema of swine. Knowles NJ (2004). Vesicular exanthema of swine. Surveillance 15(4), 13-14. In: Coetzer JAW , Tustin RC (eds.) Infectious Diseases of Livestock. Oxford University Press, Cape Town. Pp. Iowa State University (2011). College of Veterinary 700-702. Medicine. Vesicular exanthema of swine (San Miguel sea lion viral disease). Available at: Madin SH and Traum J (1955). Vesicular http: / / vetmed.iastate.edu/vdpam/new-vdpam- exanthema of swine. Bacteriological Reviews 19, 6-19. employees / food-supply-veterinary- medicine/ swine/ swine-diseases / vesicular- Torres A (2008). United States Animal Health exanthema-s , last accessed 14 September 2013. Association. Vesicular exanthema of swine. In: Foreign Animal Diseases, Boca publications group, Boca Raton. King AMQ, Adams MJ, Carstens EB and Pp. 419-422. Lefkowitz (2012). Virus Taxonomy. Ninth report o f the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London. Pp. 977-986.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 33. VESICULAR STOMATITIS VIRUS

33.1. HAZARD IDENTIFICATION 33.1.1. Aetiological agent 33.1.2. Iceland status

Family: Rhabdoviridae, Genus: Vesiculovirus, Species: Vesicular stomatitis (VS) has never been reported in Vesicular stomatitis Alagoas virus, Vesicular stomatitis Iceland and is listed as a group A notifiable disease in Indiana virus, Vesicular stomatitis New Jersey virus (Tordo Act No 25/1993 (Willeberg 2013). Ongoing freedom et al. 2005). Many authors regard the three species of is supported by general surveillance (OIE 2013). virus as serotypes of the same species. 33.1.3. European Union status

Table 24 (below) summarises the VS status of the 28 countries of the European Union based on their official returns to the OIE.

Table 24: Status of vesicular stomatitis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported January 1979 Belgium Freedom Has never occurred Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Last occurrence unknown Germany Freedom Has never occurred Greece Freedom Has never occurred Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom Has never occurred Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Freedom Has never occurred Portugal Freedom Has never occurred Romania Freedom Has never occurred Slovakia Freedom Has never occurred Slovenia Freedom Has never occurred Spain Freedom Has never occurred Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 33.1.4. Epidemiology of the hooves, teats and lymph nodes (Lubroth et al. 2006). It is not found in blood (Lubroth et al. 2006). Vesicular stomatitis is primarily an insect-borne virus but it can also be transmitted by contact (Lubroth et 33.1.5. Hazard identification conclusion al. 2006). Outbreaks of disease occur sporadically in the United States and are always associated with Meat is not a vehicle for the transmission of VS and insect transmission ( Rodriguez et al. 1996; Rodriguez this disease is not recognised in the European Union. 2002; Lubroth et al. 2006). The virus is found in VS virus is not identified as a hazard in unrestricted epithelial tissues of the mouth, nose, coronary region meat imports from the European Union.

References

Lubroth J, Rodriguez L and Dekker A (2006). Rodriguez LL, Fitch WM and Nichol ST (1996). Vesicular stomatitis. In: Straw BE, Zimmerman JJ, Ecological factors rather than temporal factors D'Allaire S, Taylor DJ (eds), Diseases of Swine. 9th dominate the evolution of vesicular stomatitis virus. edition. Blackwell Publishing, Ames, Iowa. Pp. 525­ Proceedings of the National Academy of Sciences USA 93, 535, 13030-13035.

OIE (2013). World Animal Health Information Tordo N, Benmansour A, Calisher C, Dietzgen Database (WAHID) Interface. Available at: RG, Fang R-X, Jackson AO, Kurath G, Nadin- http: / /www.oie.int/wahis 2/public/wahid.php/Wah Davis S, Tesh RB and Walker PJ (2005). Genus idhome/Home, last accessed 1 July 2103. Vesiculovirus. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds), Eighth Report of the Rodriguez LL (2002). Emergence and re-emergence International Committee on Taxonomy of Viruses. Elsevier of vesicular stomatitis in the United States. Virus Academic Press, Amsterdam. Research 85, 211-219. W illeberg P (2013). Chapter 5. Notification and animal disease surveillance. In: Risk assessments regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 34. BACILLUS ANTHRACIS

34.1. HAZARD IDENTIFICATION 34.1.1. Aetiological agent 34.1.2. Iceland status

Bacillus anthracis (the cause of anthrax) is an aerobic, Anthrax was last reported in Iceland in 2004 and is spore-forming bacillus. The bacilli (vegetative form) listed as a group A notifiable disease in Act No survive poorly outside the animal host, but the spores 25/1993 (Willeberg 2013). Ongoing freedom is which form in the presence of oxygen are very supported by general surveillance (OIE 2013). resistant, and able to withstand adverse environmental conditions for many years (National Center for Biotechnology Information 2011). 34.1.3. European Union status

Table 25 (below) summarises the anthrax status of the 28 countries of the European Union based on their official returns to the OIE.

Table 25: Status of anthrax in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Freedom Last reported 1988 Belgium Freedom Last occurrence unknown B ulgaria Present Restricted to certain zones Croatia Present Clinical disease Cyprus Freedom Last reported 1969 Czech Republic Freedom Last reported 1977 Denmark Freedom Last reported 1988 Estonia Freedom Last reported 1996 Finland Freedom Last reported November 2008 France Freedom Last reported September 2009 Germany Present Clinical disease Greece Present Restricted to certain zones Hungary Present Restricted to certain zones Ireland Freedom Last reported 1970 Italy Present Clinical disease Latvia Freedom Last reported January 1989 Lithuania Freedom Last reported 1998 Luxembourg Freedom Last occurrence unknown Malta Freedom Last reported 1974 Netherlands Freedom Last reported 1994 Poland Freedom Last reported 2001 Portugal Freedom Last occurrence unknown Romania Freedom Last reported October 2011 Slovakia Present Restricted to certain zones Slovenia Freedom Last reported October 2008 Spain Freedom Last reported 2004 Sweden Freedom Last reported September 2011 United Kingdom Freedom Last reported June 2006

34.1.4. Epidemiology contagious (Taylor 2006). Bacilli sporulate when blood from an infected animal carcase is exposed to air, and the resulting spores can remain viable in soil Anthrax is generally an acute bacterial infection of for many years (Turner et aL 1999a; Turner et aL many warm-blooded species, with pigs more resistant 1999b; De Vos and Turnbull 2004). to infection than ruminants (Taylor 2006). Animals become infected by the oral route by spores which occur in the soil although infected animals are not Anthrax can present as pharyngeal, intestinal, or septicaemic forms in pigs. The first two syndromes

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union may be mild and animals may recover spontaneously, after they have been fed raw meat from contaminated whereas the septicaemic form is usually an acute or carcasses (Moore and Greene 2006). Ingestion of peracute infection and death may occur without any large numbers of bacilli in infected meat is required prior signs being observed (Taylor 2006). to infect cats, dogs, and pigs.

Diagnosis is made by identification of the organism The lethal dose of B.anthracis varies between species, in blood smears taken from dead animals, or if the with the LD5012 ranging from < 10 spores in carcass has been opened from lymph nodes, spleen susceptible herbivores to > 107 spores in more or kidney. The organism can be cultured from blood resistant species when administered parenterally (i.e. or tissues. injected). However, B. anthracis is not an invasive organism and much higher doses are required to In Europe, many outbreaks of anthrax have been infect an individual orally, even in species regarded as attributed to the importation of raw animal products, susceptible. Large numbers of anthrax bacilli or of but contaminated food is rarely a source of infection spores may be given by mouth to laboratory animals in developed countries. However, in developing without causing infection, and anthrax spores countries, infection in humans from handling or enclosed in small gelatin capsules may be swallowed eating undercooked meat of animals that have died of by mice and guinea-pigs without harm, although anthrax occurs periodically (MacDiarmid 1991). virulent spores can be recovered from the faeces for a Apart from ingestion of contaminated materials, week. Similarly, in a study on 50 pigs given doses of infection through skin wounds and abrasions may 107—1010 spores in feed containing grit, the majority also occur and is the principal route of infection for showed clinical illness with recovery, and just two humans (De Vos and Turnbull 2004). In some died with confirmed anthrax 6 and 8 days respectively circumstances, human infection can occur by after ingestion of the spores; these were estimated to inhalation (woolsorter’s disease). have received 1.6 x 107 and 7.8 x 107 spores respectively (World Health Organisation 2008). 34.1.5. Hazard identification conclusion Considering the very low likelihood that infected animals would pass ante-mortem and post-mortem Historically, outbreaks of anthrax have been inspection, it is highly unlikely that there would be associated with imported animal products. sufficient bacilli present in meat derived from such Accordingly, Bacillus anthracis is identified as a individuals to transmit infection via the oral route. potential hazard in imported meat and meat products. The likelihood of exposure is therefore assessed to be negligible. 34.2. RISK ASSESSMENT 34.2.1. Entry assessment 34.2.3. Risk estimation

Although anthrax is a relatively rare disease, it occurs Since the exposure assessment is negligible, the risk is sporadically within the European Union. estimated to be negligible and Bacillus anthraas is not assessed to be a risk in unrestricted meat imports Animals that are acutely infected with anthrax would from the European Union. be expected to exhibit obvious and severe clinical signs. Such animals would not pass ante-mortem and post-mortem inspection. If infected animals were to go unnoticed, they would be incubating disease or possibly carrying spores in their intestines. However, there is no evidence that anthrax is transmitted by animals before the onset of clinical and pathological signs (Creel 1995).

The likelihood that meat commodities contain contaminated tissues that have been sourced from animals that passed ante-mortem and post-mortem inspections is assessed as extremely low.

34.2.2. Exposure assessment

Anthrax is naturally a disease of herbivores with pigs, dogs, and cats being relatively resistant. Isolated infections in these species have been reported during 12 LD50 is the amount of an agent that is sufficient to kill 50 percent major anthrax outbreaks in livestock. Infections in of a population of animals usually within a certain time captive canids and felids have also been reported

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union References

Centers for Disease Control and Prevention OIE (2013). World Animal Health Information (2011). Gastrointestinal anthrax. Available at: Database (WAHID) Interface. Available at: http://emergency.cdc.gov/agent/anthrax/gi/, last http://www.oie.int/wahis 2/public/wahid.php/Wah accessed 26 September 2013. idhome/Home, last accessed 1 July 2103.

Creel S (1995). The effects of anthrax on endangered Taylor DJ (2006). Miscellaneous bacterial infections. African wild dogs (Lycaon pictus). The Zoological Society of Anthrax. In: Straw BE, Zimmerman JJ, D'Allaire S, London 236 199-209. Taylor DJ (eds), Diseases of Swine. 9th edition. Blackwell Publishing, Ames, Iowa. Pp. 817-822 De Vos V and Turnbull PCB (2004). Anthrax. In: Coetzer JAW, Tustin RC (eds), Infectious Diseases of Turner AJ, Galvin JW, Rubira RJ, Condron RJ Livestock, Vol. 3. Oxford University Press, Cape and Bradley T (1999a). Experiences with Town. Pp. 1788-1818. vaccination and epidemiological investigations on an anthrax outbreak in Australia. Journal of Applied MacDiarmid SC (1991). The importation into New Microbiology 87, 294-297. Zealand of meat and meat products. A review of the risks to animal health. Ministry of Agriculture and T urner AJ, Galvin JW, Rubira RJ and Miller GT Fisheries New Zealand, Wellington, New Zealand. (1999b). Anthrax explodes in an Australian summer. Available at: Journal of Applied Microbiology 87, 196-199. http: / / www.biosecurity.govt.nz / files / regs / imports / r isk/meat-meat-products-ra.pdf, last accessed 2 W illeberg P (2013). Chapter 5. Notification and September 2013. animal disease surveillance. In: Risk assessments regarding open trade in live animals to Iceland. Icelandic Moore GE and Greene CE (2006). Anthrax. In: Food and Veterinary Authority (MAST), Reykjavik, Greene CE (ed) Infectious Diseases o f the Dog and Cat. Iceland. Pp. 59-90. Elsevier, St. Louis. Pp. 312-315. World Health Organisation (2008). Anthrax in National Center for Biotechnology Information humans and animals, 4th Edition. WHO Press, (2011). Bacillus anthracis. [Online] Available at: Geneva. http: / / www.ncbi.nlm.nih.gov/Taxonomy/Browser/ wwwtax.cgi?mode=Infoandid=1392andlvl=3andlin= fandkeep=1andsrchmode=1andunlock, last accessed 17 August 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 35. BRUCELLA SPP.

35.1. HAZARD IDENTIFICATION 35.1.1. Aetiological agent 35.1.2. Iceland status

Brucella are coccobacilli or short rods measuring from Brucellosis has never been reported in Iceland. 0.6 to 1.5 gm long and from 0.5 to 0.7 gm wide. Brucellosis due to B. abortus, B. melitensis, or B. suis is They are usually arranged singly, and less frequently listed as a group A notifiable disease in Act No in pairs or small groups. The morphology of Brucella 25/1993 and ovine epididymitis is listed as a group B is fairly constant, except in old cultures where notifiable disease. A serological survey for B. abortus pleomorphic forms may be evident. Brucella are was carried out in cattle in 1993 and systematic nonmotile. They do not form spores, and flagella, surveillance has been in place since 2007. A pili, or true capsules are not produced. Brucella are serological survey of sheep for B. melitensis was carried Gram negative and usually do not show bipolar out in 2010 (Willeberg 2013). staining (Nielsen and Ewalt 2009). This Chapter addresses infection of cattle, sheep, goats, or pigs Ongoing freedom from brucellosis due to B. abortus with Brucella abortus, B. melitensis, B. ovis, or B. suis. or B. melitensis is supported by general and targeted surveillance. Ongoing freedom from brucellosis due Bovine brucellosis is usually caused by Brucella abortus, to B. suis is supported by general surveillance (OIE less frequently by B. melitensis, and occasionally by B. 2013). suis (Nielsen and Ewalt 2009). 35.1.3. European Union status Brucella melitensis (biovars 1, 2, or 3) is the main cause of caprine and ovine brucellosis. Tables 26, 27, 28, and 29 (below) summarise the status of the 28 countries of the European Union Sporadic cases caused by B. abortus have been with regard to brucellosis (due to B. abortus, B. observed, but cases of natural infection are rare in melitensis, and B. suis), and ovine epididymitis (due to sheep and goats. (Garin-Bastuji and Blasco 2009a). B. ovis) based on their official returns to the OIE. Brucella ovis produces a clinical or subclinical disease in sheep that is characterised by genital lesions in rams (ovine epididymitis), and placentitis in ewes (Garin- Bastuji and Blasco 2009b).

Brucellosis in pigs is caused by Brucella suis. The species Brucella suis consists of five biovars, but the infection in pigs is caused by B. suis biovars 1, 2, or 3 (Olsen 2009).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 26: Status of bovine brucellosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported March 2008 Belgium Present No clinical disease Bulgaria Freedom Last reported 1958 Croatia Freedom Last reported 1965 Cyprus Freedom Last reported 1932 Czech Republic Freedom Last reported 1964 Denmark Freedom Last reported 1962 Estonia Freedom Last reported 1961 Finland Freedom Last reported 1960 France Present Disease restricted to certain zones Germany Freedom Last reported 2004 Greece Present Clinical disease Hungary Freedom Last reported 1985 Ireland Freedom Last reported 2006 Italy Present Disease restricted to certain zones Latvia Freedom Last reported 1963 Lithuania Freedom Last reported 1992 Luxembourg Freedom Last reported 1995 Malta Freedom Last reported 1996 Netherlands Freedom Last reported 1996 Poland Freedom Last reported 2008 Portugal Present Disease limited to one or more zones Romania Freedom Last reported 1963 Slovakia Freedom Last reported 1964 Slovenia Freedom Last reported 1961 Spain Present Disease restricted to certain zones Sweden Freedom Last reported 1957 United Kingdom Present Clinical disease

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 27: Status of ovine and caprine brucellosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported January 2009 Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 2009 Croatia Freedom Last reported December 2010 Cyprus Freedom Last reported October 2010 Czech Republic Freedom Has never occurred Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Present Restricted to certain zones Germany Freedom Last reported June 2006 Greece Present Restricted to certain zones Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Present Restricted to certain zones Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Last reported August 2008 Netherlands Freedom Has never occurred Poland Freedom Has never occurred Portugal Present Clinical disease Romania Freedom Has never occurred Slovakia Freedom Last occurrence unknown Slovenia Freedom Has never occurred Spain Present Restricted to certain zones Sweden Freedom Last reported 1957 United Kingdom Freedom Last reported 1956

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Table 28: Status of porcine brucellosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported July 2010 Belgium Present No clinical disease Bulgaria Freedom Last reported 2005 Croatia Freedom Last reported March 2012 Cyprus Freedom Last occurrence unknown Czech Republic Freedom Last occurrence unknown Denmark Freedom Last reported 1999 (domestic); 2002 (wild) Estonia Freedom Last reported 1988 Finland Freedom Has never occurred France Present Clinical disease Germany Freedom Last reported December 2011 Greece Freedom Last reported 2001 Hungary Present Disease restricted to certain zones Ireland Freedom Has never occurred Italy Present Disease restricted to certain zones Latvia Freedom Last reported December 2010 (domestic); June 2011 (wild) Lithuania Freedom Last reported 1992 Luxembourg Freedom Last occurrence unknown Malta Freedom Has never occurred Netherlands Freedom Last reported 1973 Poland Freedom Last reported 2003 Portugal Freedom Last reported June 2009 (domestic); June 2011 (wild) Romania Freedom Last reported 2009 Slovakia Freedom Last reported 1992 Slovenia Freedom Last occurrence unknown Spain Present Disease restricted to certain zones Sweden Freedom Last reported 1957 United Kingdom Freedom Has never occurred

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 29: Status of ovine epididymitis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther A ustria Present Clinical disease Belgium Freedom Last occurrence unknown B ulgaria Present Clinical disease C roatia Present No clinical disease Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 2004 Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Present Disease restricted to certain zones Germany Freedom Last reported 1986 Greece Freedom Last occurrence unknown Hungary Freedom Last reported June 2009 Ireland Freedom Has never occurred Italy Freedom Last occurrence unknown Latvia Freedom Last reported July 1989 Lithuania Freedom Has never occurred Luxembourg Freedom Last occurrence unknown Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Freedom Last occurrence 2004 Portugal Freedom Last reported 1995 R om ania Present No clinical disease Slovakia Freedom Last occurrence 2006 Slovenia Freedom Last reported August 2008 Spain Present Disease restricted to certain zones Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

35.1.4. Epidemiology Susceptibility to infection with Brucella spp. is influenced by age, sex, and reproductive status. For example, sexually mature, pregnant cattle are more Although bovine brucellosis formerly had a world­ susceptible to infection than sexually immature cattle wide distribution, it has now been eradicated from of either sex (Radostits et al. 2007a). Sexually many developed countries. The bacterium is an immature cattle generally do not become infected economically important cause of abortion in cattle following exposure, or recover quickly. However, and still occurs, but at a low prevalence, in some parts bulls occasionally become infected in utero or by the of the European Union. B. melitensis causes abortion oral route and retain infection in their testes in goats primarily but also sheep, and occurs in some (Godfroid et al. 2004b; Radostits et al. 2007a). countries in Europe. B. suis is an important cause of reproductive losses in pigs and occurs in some European countries. B. melitensis infections are usually associated with sheep and goats but there are occasional reports of infection in cattle, dogs, and (rarely) horses and pigs Brucella spp. are primarily associated with their (Center Food Security and Public Health 2009a; specific maintenance hosts, although infections may Center Food Security and Public Health 2009b). B. also occur in other species in close contact with suis is primarily associated with domestic and wild or infected animals. For instance, the maintenance feral pigs but infection has been reported occasionally hosts for B. abortus include cattle, buffalo, and elk. in cattle, small ruminants, horses, dogs, and other However, a variety of other animals can become spillover hosts (Center Food Security and Public “spillover hosts” where this organism is enzootic. B. Health 2009c). abortus has been reported in many animals including sheep, goats, pigs, horses, and dogs. However, horses are considered dead-end hosts and disease in Brucellosis is a venereal disease in pigs, with sows dogs is self-limiting so these animals are not readily infected when mated with infected boars or important in the spread and maintenance of B. inseminated with semen containing B. suis (MacMillan abortus, B. melitensis, or B. suis (Garin-Bastuji et al. et al. 2006). Apart from domestic pigs, reservoirs of 2009). B. suis infection are recognised in European hares

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union (Bendtsen et al. 1954) and feral pigs (Drew et al. 35.1.5. Hazard identification conclusion 1992). Transmission of infection from wild boars to domestic pigs is thought to be through the venereal Meat is recognised as a vehicle for the introduction of route. Waste feeding of hare offal has also been a number of Brucella spp. that are present in the implicated as a method of introduction (Algers et al. European Union. Brucella spp. are identified as a 2009). potential hazard in imported meat and meat products.

Infection with B. suis is associated with reproductive 35.2. RISK ASSESSMENT failure characterised by abortion, stillbirth, infertility, and testicular lesions. B. suis localises to the placenta 35.2.1. Entry assessment of pregnant sows, leading to placentitis with subsequent malnutrition and hypoxia, and abortion in Brucellae are resistant to pickling and smoke curing mid-to-late pregnancy (Algers et al. 2009). However, so it is likely that certain meat products could harbour the clinical evidence of infection varies considerably the organism. For example, B. abortus has been between herds and clinical signs may be only shown to survive in meat and salted meat for 65 days transient or absent. Death is rare (MacMillan et al. at 0°C-20°C and up to 175 days in sausage 2006). (MacDiarmid and Thompson 1997). Similarly, B. melitensis survived in hams of naturally infected pigs In animals, brucellosis is primarily transmitted by for at least 21 days. In frozen meat Brucellae may contact with the placenta, foetus and birth fluids survive up to 2 years (MacMillan et al. 2006). from infected animals (Radostits et al. 2007a). Because Brucellae could be present in meat and Humans generally contract brucellosis by drinking particularly in organs such as liver, kidneys, lymph unpasteurised milk or eating contaminated dairy nodes, testes, udders and bone marrow (Garin-Bastuji products (Godfroid et al. 2004a; Center Food Security et al. 2009; Acha and Szyfres 2003) the likelihood of and Public Health 2009a). Occupational exposure entry is assessed to be non-negligible. occurs when individuals such as farmers and veterinarians contact infectious discharges at parturition and the organism may gain entry via the 35.2.2. Exposure assessment mucous membranes or abraded skin. Hunters and abattoir workers may also be at risk of becoming Contaminated raw meat fed to dogs may cause infected whilst preparing carcasses of infected infection. Cats, in contrast, are highly resistant and animals (Godfroid et al. 2004a; Radostits et al. 2007a). unlikely to be infected (Greene and Carmichael Porcine brucellosis is a significant public health 2006). In dogs, infection is self-limiting and they are concern, with occupational B. suis infections not considered important in the epidemiology of the described in farmers, veterinarians, abattoir workers, spread and maintenance of infection. However, and individuals who have direct contact with feral contaminated pet food could have the potential to swine (MacMillan et al. 2006). expose many dogs.

MacDiarmid and Thompson (1997) concluded that For cattle, goats, sheep or deer to become infected under certain circumstances meat may serve as a they would have to be exposed to contaminated vehicle for brucella species. Their review noted that meat. Since herbivorus animals would be unlikely to humans have become infected from eating raw bone naturally eat meat, the likelihood of exposure by this marrow or raw meat of animals infected with B. suis. pathway is negligible. It is more plausible that In frozen meat, survival of the organism for several exposure would happen through feeding raw meat to years has been reported (MacDiarmid and Thompson pigs. 1997). The FAO considers food-borne infection rarely occurs in humans from eating raw meat from Although there are a small number of commercial pig infected animals (Robinson 2003). farms in Iceland, there has been an increase in the number of people keeping a small number of pigs as More recently, an OIE ad hoc Group noted that other a ‘hobby’. In addition there has been an increase in raw meat or meat products from animals from herds the number of sheep or cattle farms that keep a small not free from brucellosis and especially from animals herd of pigs. Although it is unlikely that commercial being eliminated in the framework of eradication pig farms in Iceland would use kitchen waste as a activities should not enter international trade. This is source of feed, it is highly likely that kitchen waste because some organs (liver, spleen, kidneys, lymph would be used as an inexpensive source of feed for nodes, testes, and udder) may pose a human health pigs in small hobby herds. risk due to contamination with Brucellae, particularly if used or consumed unprocessed (Garin-Bastuji et al. No reports of outbreaks of pigs naturally infected 2009). from eating raw meat could be found. Therefore, the frequency of exposure and infection by this route is obviously very low. Moreover, MacMillan et al. 2006 does not cite feeding raw meat to pigs as a means of

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union transmitting infection. In contrast, Radostits et aL animals in close contact, (including different species) (2007b) claim that feeding kitchen waste containing exposed to the placenta, aborted foetus, and fluids raw infected pig meat presents a risk. are at risk of infection. In addition, infected animals pose a public health risk for people occupationally Eating raw meat is a rare cause of foodborne exposed to them, their birth products, carcasses or infection in humans and animals. This is particularly tissues. For example, dairy farmers, dog breeders, the case for humans eating wild boar and feral veterinarians, pig farmers, and abattoir workers. pigmeat (Radostits et aL 2007a). In humans, brucellosis is primarily an occupational disease Movement of infected animals could spread the (Godfroid et al. 2004a). The FAO considers food- disease and the organism could become endemic. borne infection rarely occurs from eating raw meat This would lead to production losses affecting from infected animals (Robinson 2003). Further, the individual farmers which could eventually translate to United States Department of Agriculture states “there significant deterioration in national production. is no danger from eating properly cooked meat Eradication of the disease would be necessary to products because the disease-causing bacteria are not prevent ongoing production losses and sporadic cases normally found in muscle tissue and they are killed by of debilitating human disease. Such a campaign could proper cooking temperatures” (United States be expensive depending on how far the disease had Department of Agriculture 2007). spread.

However, the likelihood of exposure is assessed to be The consequences of brucellosis in humans and non-negligible since humans, pigs and dogs could be animals are assessed to be non-negligible. exposed to Brucellae in contaminated meat. 35.2.4. Risk estimation 35.2.3. Consequence assessment Since entry, exposure, and consequence assessments Consuming infected meat could transmit infection to are non-negligible, the risk estimation is non- dogs, pigs, or humans. The most common clinical negligible and Brucella spp. is assessed to be a risk in signs in animals are abortion and stillbirths. Other unrestricted meat imports from the European Union.

References

Acha PN and Szyfres B (2003). Brucellosis. In: Center Food Security and Public Health (2009b). Zoonoses and Communicable Diseases Common to Man and Ovine and caprine brucellosis:Br»cella melitensis. Animals (3rd edn.) Pan American Health Organization, Available at: Washington D.C. http: / / www.cfsph.iastate.edu/Factsheets / pdfs/bruce llosis melitensis.pdf , last accessed 19 August 2013. Algers B, Blokhuis HJ, Bøtner A, Broom DM, Costa P, Domingo M, Greiner M, Hartung J, Center Food Security and Public Health (2009c). Koenen F, Müller-Graf C, Mohan R, Morton DB, Porcine and rangiferine brucellosis: Brucella suis. Osterhaus A, Pfeiffer DU, Roberts RU, Sanaa M, Available at: Salman M, Sharp JM , Vannier P and Wierup M http: / / www.cfsph.iastate.edu/Factsheets / pdfs/bruce (2009). Scientific Opinion of the Panel on Animal llosis suis.pdf , last accessed 19 August 2013. Health and Welfare (AHAW) on a request from the Commission on porcine brucellosis (Brucella suis). The Drew ML, Jessup DA, Burr AA and Franti CE EFSA Journal 1144, 1-112. (1992). Serological survey for brucellosis in feral swine, wild ruminants, and black bear of California. Bendtsen H, Christiansen M and Thomsen A Journal of Wildlife Diseases 28, 355-363. (1954). Brucella enzootics is swine herds in Denmark — Presumably with hare as a source of infection. Garin-Bastuji B and Blasco JM (2009a). Chapter Nordisk veterinaermedicin 6, 11-21. 2.7.2. Caprine and ovine brucellosis (excluding Brucella ovis). In: OIE Manual of Diagnostic Tests and Center Food Security and Public Health (2009a). Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: Bovine brucellosis: Brucella abortus. Available at: http://www.oie.int/fileadmin/Home/eng/Health st http: / / www.cfsph.iastate.edu/Factsheets/pdfs/bmce andards /tahm/2.07.02 CAPRINE OVINE BRUC. llosis abortus.pdf , last accessed 19 August 2013. pdf, last accessed 1 July 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Garin-Bastuji B and Blasco JM (2009b). Chapter OIE (2013). World Animal Health Information 2.7.9. Ovine epididymitis {Brucella ovis). In: OIE Database (WAHID) Interface. Available at: Manual o f Diagnostic Tests and Vaccinesfo r Terrestrial http://www.oie.int/wahis 2/public/wahid.php/Wah Animals, OIE, Paris. Available at: idhome/Home, last accessed 1 July 2103. http://www.oie.int/fileadmin/Home/eng/Health st andards /tahm/2.07.09 OVINE EPID.pdf last Olsen S (2009). Chapter 2.8.5. Porcine brucellosis. accessed 1 July 2013. In: OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, OIE, Paris. Available at: Garin-Bastuji B, Nicola AM, Blasco C, Ekron http: //www.oie.int/fileadmin/Home/eng/Health st MD, Nicola AM, Hilan C, Gordejo FJR and andards/tahm/2.08.05 PORCINE BRUC.pdf, last Domenech J (2009). Report of the Meeting of the accessed 4 July 2013. OIE ad hoc Group on Brucellosis. OIE Terrestrial Animal Health Standards Commission, Paris, 24-26 Radostits OM, Gay CC, Hinchcliff KW and November 2009. Available at: Constable PD (2007a). Brucellosis associated with http: / /www.oie.int/doc/ged/D7053.PDF, last Brucella abortus (Bang's disease). In: Veterinary Medicine, accessed 19 August 2013. Elsevier, Edinburgh. Pp. 966-984.

Godfroid J, Bosman PP, Herr S and Bishop GC Radostits OM, Gay CC, Hinchcliff KW and (2004a). Bovine brucellosis. In: Infectious Diseases of Constable PD (2007b). Brucellosis associated with Livestock, Oxford University Press, Cape Town. Pp. Brucella suis in pigs. In: Veterinary Medicine, Elsevier, 1510-1527. Edinburgh. Pp. 988-991.

Godfroid J, Thoen CO and Angus RD (2004b). Robinson A (2003). Guidelines for coordinated Brucella suis infection. In: Infectious Diseases of Livestock, human and animal brucellosis surveillance. FAO, Oxford University Press, Cape Town. Pp. 1542-1545. Rome. Available at: http: / / www.fao.org/docrep /006/Y4723E/y4723e00 Greene CE and Carmichael LE (2006). Canine .htm#Contents. last accessed 19 August 2013. brucellosis. In :Greene CE (ed.) Infectious Diseases of the Dog and Cat. Elsevier; St. Louis, USA. Pp. 369-381. United States Departement of Agriculture (2007). Questions and answers about brucellosis. US MacDiarmid SC and Thompson EJ (1997). The Department of Agriculture, Animal and Plant Health potential risks to animal health from imported sheep Inspection Service. Available at: and goat meat. In: Revue Scientifique et Technique Office http: / /www.aphis.usda.gov/publications /animal hea International des Épizooties 16, 45-56. lth/content/printable version/faq brucellosis.pdf , last accessed 26 September 2013. MacMillan AP, Schleicher H, Korslund J and Stoffregen WC (2006). Brucellosis. In: Straw BE, W illeberg P (2013). Chapter 5. Notification and Zimmerman JJ, D'Allaire S, Taylor DJ (eds), Diseases animal disease surveillance. In: Risk assessments o f Swine. 9th edition, Blackwell Publishing, Ames, regarding open trade in live animals to Iceland. Icelandic Iowa. Pp. 603-11, Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90. Nielsen K and Ewalt DR (2009). Chapter 2.4.3. Bovine brucellosis. In: OIE Manual of Diagnostic Tests and Vaccinesfor Terrestrial Animals, OIE, Paris. Available at: http://www.oie.int/fileadmin/Home/eng/Health st andards /tahm/2.04.03 BOVINE BRUCELL.pdf, last accessed 1 July 2013

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 36. CHLAMYDOPHILA ABORTUS

36.1. HAZARD IDENTIFICATION 36.1.1. Aetiological agent 36.1.2. Iceland status

Ovine chlamydiosis (enzootic abortion of ewes Enzootic abortion (EAE) has never been reported in [EAE] or ovine enzootic abortion [OEA]) is caused Iceland and is listed as a group A notifiable disease in by the bacterium Chlamydophila abortus. Act No 25/1993 (Willeberg 2013). Ongoing freedom Taxonomically, the family Chlamydiaceae has been is supported by general surveillance (OIE 2013). divided into two genera and nine species based on sequence analysis of the 16s and 23s rRNA genes. The genus Chlamydia includes C. trachomatis (humans), 36.1.3. European Union status C. suis (swine) and C. muridarum (mouse and hamster). The genus Chlamydophila includes C. psittaci (avian), Table 30 (below) summarises the EAE status of the C.felis (cat), C. abortus (sheep, goat and cattle), C. caviae 28 countries of the European Union based on their (guinea-pig), the former species C. pecorum (sheep and official returns to the OIE. cattle) and C. pneumoniae (humans). A proposal has been mooted to recombine all the species in a single genus (Chlamydia) (Everett et al. 1999; Sachse and Longbottom 2012).

Table 30: Status of enzootic abortion of ewes in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last reported 2004 (domestic); 2011 (wild) Bulgaria Not reported Croatia Freedom Last occurrence unknown Cyprus Freedom Last reported June 2012 Czech Republic Freedom Last reported 1999 Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Present Clinical disease Germany Present Clinical disease Greece Present Restricted to certain zones Hungary Present Restricted to certain zones Ireland Present Clinical disease Italy Present Restricted to certain zones Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Last reported 2003 Netherlands Present Clinical disease Poland Not reported Portugal Present Clinical disease Romania Freedom Last occurrence unknown Slovakia Freedom Last reported March 2011 Slovenia Freedom Last reported June 2010 Spain Present Clinical disease Sweden Freedom Last reported 2003 United Kingdom Present Clinical disease

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 36.1.4. Epidemiology Ewes that have aborted remain long-term intestinal carriers (Aitken 1983) and may also be chronically infected in their reproductive tract (Papp et aL 1994; Enzootic abortion caused by C. abortus is primarily a Papp et aL 1998). Michalopolou et aL (2007) report disease of sheep and goats (Aitken 1983) although the nearly 50% of 304 cull sheep uteri from a United pathogen is also recognised to infect cattle, causing Kingdom abattoir were positive (by polymerase chain epizootic bovine abortion. Infection of deer is also reaction) for C. abortus. Although these results (less commonly) described (Sachse and Longbottom indicate organism persistence in the uterus of sheep, 2012). C. abortus is rarely zoonotic and may cause the authors noted the sheep may not pose any abortion in women who have been in contact with transmission risk because of PCR sensitivity. Recent infected ewes during the lambing season (Center for evidence suggests that the proportion of infectious Food Security and Public Health 2005; Sachse and ewes is reduced following breeding season since only Longbottom 2012). A single case of C. abortus in an low levels of Chlamydial DNA are detected at abattoir worker has been described (Hadley et aL subsequent lambing (Sachse and Longbottom 2012). 1992).

There is no evidence that eating meat transmits Transmission in animals occurs by direct contact via infection to animals or humans (Anderson 2004; the faecal-oral and venereal routes. Within a flock, Center for Food Security and Public Health 2005; the primary source of infection is the placenta and Radostits 2007). An OIE review did not identify C. the uterine discharges of aborting ewes. Subsequent abortus as a potential hazard associated with trade in transmission occurs through ingestion of organisms sheep and goat meat (MacDiarmid and Thompson shed in large quantities in vaginal fluids and placental 1997). membranes at abortion or lambing. The environment becomes contaminated and the organism may survive several days on pasture and 36.1.5. Hazard identification conclusion longer in cold weather (Radostits 2007). There is no evidence to suggest that imported meat The incubation period of C. abortus infections in or meat products may act as a vehicle for sheep varies. Some animals become infected in one Chlamydophila abortus. Accordingly this organism is season, remain infected and abort in the subsequent not identified as a hazard in unrestricted meat season, whilst others may abort in the same season as imports from the European Union. infection (Aitken 1983).

References

Aitken ID (1983). Enzootic (Chlamydial) abortion. Hadley KM, Carrington D, Frew CE, Gibson AA In: Martin WB (eds) Diseases o f Sheep. Oxford, and Hislop WS (1992). Ovine chlamydiosis in an Blackwell Scientific Publications. Pp. 119-123 abattoir worker. Journal of Infection 25 (Suppl 1), 105­ 109. Andersen AA (2004). Chlamydiosis. In: Coetzer JAW, Tustin RC (eds) Infectious Diseases o f Livestock. MacDiarmid SC and Thompson EJ (1997). The Oxford, Oxford University Press. Pp. 550-564. potential risks to animal health from imported sheep and goat meat. Revue Scientifique et Technique Office Center for Food Security and Public Health International des Épiyooties 16, 45-56. (2005). Zoonotic Chlamydiae from mammals. Available at: Michalopolou E, Leigh AJ and Cordoba LG http: / / www.cfsph.iastate.edu /Factsheets / pdfs/ chla (2007). Detection of the genome of Chlamydophilia mydiosis.pdf , last accessed 19 August 2013. abortus in samples taken from the uteri of 304 sheep at an abattoir. Veterinary Record 161, 153-155. Everett KDE, Bush RM and Andersen AA (1999). Emended description of the order Chlamydiales, OIE (2013). World Animal Health Information proposal of Parachlamydiaceae fam. nov. and Database (WAHID) Interface. Available at: Simkaniaceae fam. nov., each containing one http://www.oie.int/wahis 2/public/wahid.php/Wah monotypic genus of the family Chlamydiaceae, idhome/Home, last accessed 1 July 2103. including a new genus and five new species, and standards for the identification of organisms. Papp JR, Shewen PE and Gartley CJ (1994). International Journal o f Systematic Bacteriology 49, 415-440. Abortion and subsequent excretion of chlamydiae from the reproductive tract of sheep during oestrus. Infection and Immunity 62, 3786-3792.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Papp JR, Shewen PR, Thorn CE and Andersen Sachse K and Longbottom D (2012). Chapter 2.7.7. AA (1998). Immunocytological detection of Enyootic abortion of ewes (ovine chlamydiosis). In: OIE Chlamydiumpsittaci from cervical and vaginal samples Manual of Diagnostic Tests and Vaccines for of chronically infected ewes. Canadian Journal of Terrestrial Animals, OIE, Paris. Available at: Veterinary Research 62, 72-74. http: //www.oie.int/fileadmin/Home/eng/Health st andards/tahm/2.07.07 ENZ ABOR.pdf, last Radostits OM, Gay CC, Hinchcliff KW and accessed 1 July 2013. Constable PD (2007). Chlamydophila abortion (enzootic abortion of ewes, ovine enzootic abortion). W illeberg P (2013). Chapter 5. Notification and In: Veterinary Medicine. Elsevier, Edinburgh. Pp. 1435­ animal disease surveillance. In: Risk assessments 1437. regarding open trade in live animals to Iceland. Icelandic Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 37. COXIELLA BURNETII

37.1. HAZARD IDENTIFICATION 37.1.1. Aetiological agent 37.1.2. Iceland status

Coxiella burnetii is a Gram-negative obligate Q fever has never been reported in Iceland and is intracellular bacterium, adapted to thrive within the listed as a group B notifiable disease in Act No phagolysosome of the phagocyte. Although 25/1993. Serological surveillance for Q fever was historically classified in the Rickettsiaceae family, initiated in 2012 (Willeberg 2013). Ongoing freedom phylogenetic analysis of the 16s rRNA sequence has is supported by general surveillance (OIE 2013). shown that the Coxiella genus is distant from the Rickettsia genus. Coxiella burnetii has been placed in the Coxiellaceae family in the order Legionellales of the 37.1.3. European Union status gamma subdivision of Proteobacteria (Rousset et al. 2010). Table 31 (below) summarises the Q fever status of the 28 countries of the European Union based on their official returns to the OIE. Table 31: Status of Q fever in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Not reported Belgium Freedom Last reported 2009 B ulgaria Present Infection in one or more zones C roatia Present Clinical disease Cyprus Present Clinical disease Czech Republic Freedom Last reported 1996 Denmark Present Disease suspected Estonia Freedom Has never occurred Finland Freedom Last reported June 2012 France Present Disease restricted to certain zones Germany Present Clinical disease Greece Freedom Last reported December 2011 Hungary Present Disease restricted to certain zones Ireland Present Clinical disease Italy Present Disease restricted to certain zones Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Present No clinical disease Malta Reported April 2013 Previously had never occurred Netherlands Present No clinical disease Poland Present No clinical disease Portugal Freedom Last reported December 2011 Romania Freedom Last occurrence unknown Slovakia Freedom Last reported May 2011 Slovenia Freedom Last reported June 2010 Spain Present Clinical disease Sweden Present Disease suspected United Kingdom Present Clinical disease

37.1.4. Epidemiology C. burnetii probably infects all mammals, birds, and many arthropods (Marrie 1990; Marin and Raoult 1999). Infection of animals is of minimal economic Q fever occurs throughout the world, with the importance and rarely causes disease, although C. exception of New Zealand (Worthington 2001), burnetii is a zoonotic organism that may result in Iceland (OIE 2013), and possibly Norway (Jensenius sporadic abortions in both humans and animals et al. 1997). (Raoult et al. 2002; Hatchette et al. 2003). Although most human infections are asymptomatic or cause a

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union mild flu-like illness, infections sometimes result in so, infection may occur through skin abrasions while serious complications such as myocarditis, handling infected organs. Humans may, occasionally, endocarditis, hepatitis, and renal failure (Marin and become infected by eating infected food-stuffs but Raoult 1999; Woldehiwet 2004). this route of infection is uncommon (MacDiarmid 1991). Cattle, sheep, and goats are the principal source of infection for humans, with transmission primarily No transmission of C. burnetii by meat has been from inhalation of contaminated aerosols (especially reported (Pepin et al. 1997). Consistent with this, a dust contaminated by animals and their birth review of the public health hazards of meat from products) or from contact with infected uterine small ruminants concluded that Q fever was not a discharges and placentae (Behymer and Riemann foodborne disease (Adams et al. 1997). There is a 1989; Marrie 1990; Hawker et al. 1998; Marin and single report of C. burnetii surviving up to 30 days in Raoult 1999; Tissot-Dupont et al. 1999). experimentally contaminated meat stored under refrigeration (MacDiarmid 2010). Ticks may also play a role in spreading the disease and many species of tick can be infected. It has been MacDiarmid and Thompson (1997) reviewed the suggested that dried tick faeces form an infective dust risks to animal health from imported sheep and goat that can contaminate animal coats and become meat and concluded that the risk C. burnetii being aerosolised. introduced into an importing country through sheep and goat meat products was small. This review noted Infected cattle shed the organism in their milk after that there were no references describing meat as a successive parturitions and drinking unpasteurised vehicle for C. burnetii. contaminated milk may transmit infection to humans (Kelly 2004). However, this route of infection is 37.1.5. Hazard identification conclusion considered much less efficient when compared to inhalation of contaminated aerosols (Hart 1973; Q fever is primarily transmitted by airborne exposure Arricau-Bouvery and Rodolakis 2005). to contaminated birth products from aborted livestock. It is an occupational zoonoses and not a During the bacteraemic phase of the disease, C. foodborne disease. There is no evidence to indicate burnetti is carried to all organ systems. In some cattle that meat or meat products are likely to be a vehicle the agent may persist for months in liver, kidney, for introduction of this disease. C. burnetii is not muscles, lymph nodes etc. While slaughterhouse identified as a hazard in unrestricted meat imports workers are particularly at risk from Q fever, their from the European Union. exposure is usually via aerosols, not meat p er se. Even

References

Adams DB, Butler RJ and Nicholls TJ (1997). Hawker Jl, Ayres JG and Blair L (1998). A large Public health hazards of meat from small ruminants: outbreak of Q fever in the West Midlands, a the perspective of Australia. Revue Scientifique et windborne spread to a metropolitan area? Technique Office International des Épiyooties 16, 433-440. Communicable Diseases and Public Health 1, 180-187.

Arricau-Bouvery N and Rodolakis A (2005). Is Q Jensenius M, Maeland A, Kvale D, Farstad IN, fever an emerging or re-emerging zoonosis? Veterinary Vene S and Bruu AL (1997). Q-fever imported into Research 36, 327-349. Norway. Tidsskrift fo r den Norske laegeforening 117, 3937­ 3940. Behymer D and Riemann HP (1989). Coxiella burnetii infection (Q fever). Journal of the American Kelly J (2004). Q fever. In: Coetzer JAW, Tustin RC Veterinary Medical Association 194, 764-767. (eds) Infectious Diseases o f Livestock, Oxford University Press, Cape Town. Pp. 565-572. Hart RJC (1973). The epidemiology of Q fever. Postgraduate Medical Journal 49, 535-538. Marin M and Raoult D (1999). Q fever. Clinical Microbiology Reviews 12, 518-553. Hatchette T, Campbell N, Hudson R, Raoult D and Marrie TJ (2003). Natural history of Q fever in MacDiarmid SC and Thompson EJ (1997). The goats. Vector Borne Zoonotic Diseases 3, 11-15. potential risks to animal health from imported sheep and goat meat. Revue Scientifique et Technique Office International des Lpiyooties 16, 45-56.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union MacDiarmid SC (1991). The importation into New Raoult D, Fenollar F and Stein A (2002). Q fever Zealand of meat and meat products. A review of the during pregnancy: diagnosis, treatment, and follow- risks to animal health. Ministry of Agriculture and up. Archives of Internal Medicine 162, 701-704. Fisheries New Zealand, Wellington, New Zealand. Available at: Rousset E, Sidi-Boumedine K and Thiery R http: / / www.biosecurity.govt.nz/ files / regs/imports / r (2010). Chapter 2.1.12. Q fever. In: OIE Manual of isk/meat-meat-products-ra.pdf, last accessed 2 Diagnostic Tests and Vaccines fo r Terrestrial Animals, OIE, September 2013. Paris. Available at: http: //www.oie.int/fileadmin/Home/eng/Health st MacDiarmid SC (2010). Import risk analysis: Sausage andards/tahm/2.01.12 Q-FEVER.pd£ last accessed casings from small ruminants. MAF Biosecurity New 1 July 2013. Zealand, Wellington. Available at: http: / / www.biosecurity.govt.nz / files / regs / imports / r Tissot-Dupont H, Torres S and Nezri Mea isk/sausage-casings-eu-ra.pdf , last accessed 21 (1999). Hyperepidemic focus of Q fever related to August 2013. sheep and wind. American Journal of Epidemiology 150, 67-74. Marrie TJ (1990). Q fever - a review. Canadian Veterinary Journal 31, 551-563. W illeberg P (2013). Chapter 5. Notification and animal disease surveillance. In: Risk assessments OIE (2013). World Animal Health Information regarding open trade in live animals to Iceland. Icelandic Database (WAHID) Interface. Available at: Food and Veterinary Authority (MAST), Reykjavik, http: / /www.oie.int/wahis 2/public/wahid.php/Wah Iceland. Pp. 59-90. idhome/Home, last accessed 1 July 2103. Woldehiwet Z (2004). Q fever (coxiellosis): Pepin M, Russo P and Pardon P (1997). Public epidemiology and pathogenesis. Research in Veterinary health hazards from small ruminant meat products in Science 77, 93-100. Europe. Revue Scientifique et Technique Office International des Épizooties 16, 415-425. Worthington RW (2001). New Zealand is free from Q fever. Surveillance 28 (4), 3-4.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 38. LEPTOSPIRA SPP.

38.1. HAZARD IDENTIFICATION 38.1.1. Aetiological agent In domestic livestock, the clinical manifestations of leptospirosis vary from acute to subacute and chronic infections. Chronic infections localise in the kidneys The classification of leptospires is complex. Over and sometimes the genital tract, usually without 200 serovars of L. interrogans are classified causing clinical signs. Chronic infections may lead to serologically into at least 23 serogroups based on reproductive problems, such as abortion and reduced antigenic relatedness (Radostits et aL 2007). fertility in cattle and pigs. Mild infections in livestock may go unnoticed. Occasionally calves and piglets For convenience here, serovars are written as may suffer from a fatal jaundice and haemorrhagic abbreviated versions of their full technical names e.g. syndrome (Radostits et aL 2007). L. interrogans serovar pomona becomes L . pomona. Maintenance hosts may shed leptospires in their urine 38.1.2. Iceland status for months or years, sometimes in large numbers. In general, animals that are clinically affected shed more Leptospirosis has not been reported in livestock in organisms and represent a greater transmission threat Iceland. than subclinically infected animals (Greene 2006). The contamination of surface waters and mud with infected urine poses a risk of transmission to other 38.1.3. European Union status animals and humans. Infection can occur by mouth or through the skin, particularly through abrasions Leptospirosis has been diagnosed in livestock and wounds. Inapparent leptospirosis infections in throughout the European Union (Ellis and Little domestic animals may sometimes be detected only 1986). following infection of humans.

38.1.4. Epidemiology Accidental hosts usually develop overt disease and, provided they survive, recover and clear the infection Leptospirosis occurs throughout the world but is within a few weeks. Urinary excretion stops within particularly prevalent in tropical humid climates, days or a few weeks of recovery (World Health marshy or wet areas, and in regions with alkaline soils Organization 2003; Greene 2006). (Greene 2006; Ahmed et al. 2009). The endemic serovars that occur in each country differ. Leptospires may survive for a time outside the host in an environment that is damp and humid. However, Some serovars develop a commensal or, at worst, a they do not replicate outside the host and are fragile. mildly pathogenic relationships with their specific Leptospires are unable to tolerate dry conditions, animal host (‘maintenance’) species. For example, surviving less than 30 minutes in air-dried soil cattle are often associated with serovar L. hardjo and (Hunter 2004). pigs with L. pomona. Pathogenic leptospires are maintained in nature in the renal tubules of Animals that are accidental hosts are likely to display maintenance host animals where they cause very little clinical signs of disease that would be readily detected harm. However, if an animal other than a during ante-mortem and post-mortem inspection. maintenance host becomes infected it is likely to However, a maintenance host with host-adapted develop clinical disease. Such species affected in this leptospires localised in their kidneys may pass ante- manner are considered ‘accidental’ hosts. In addition, mortem and post-mortem inspections since clinical if a maintenance host for a particular serovar signs may go unnoticed. becomes infected with another serovar, it usually results in the development of clinical signs of Several species of wild mammals fed experimentally leptospirosis (Hunter 2004). infected leptospiraemic or leptospiruric mice, occasionally caused infection in the recipient (Reilly 1970). Oral infection of cattle has failed experimentally, but is suspected to occur naturally (Hunter 2004).

Ho and Blackmore (1979) showed that L. pomona survived 14 to 30 days in chilled and frozen pig kidneys. The kidneys had been collected within 20 minutes of slaughter and then slowly frozen. The periods of survival reported were considerably longer

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union than those of previous studies. This was suggested to 38.1.5. Hazard identification conclusion be because of a more sensitive culture technique employed. It was concluded that a reduction in Leptospires are fragile and requires specific numbers of leptospires occurs during chilled and environmental conditions to survive. Leptospira spp. frozen storage, but this cannot be relied upon to are not identified as a hazard in meat products since eliminate leptospires from infected kidneys. manufacturing processes and conditions inactivate leptospires. However, no transmission studies have been carried out where naturally infected, commercially derived Although chilled or frozen kidneys may harbour chilled or frozen kidneys have subsequently been fed exotic leptospires for a short time, chilling or freezing to susceptible animals and feeding fresh kidneys to temperatures are detrimental to leptospiral survival pets, for instance, is not a recognised source of and this commodity has never been implicated in the infection. Radostits et al. (2007) report that chilling international spread of leptospirosis. In their temperatures lower than 7°C and ambient extensive review, Farez and Morley (1997) did not temperatures higher than 36°C are unfavourable identify leptospirosis as a hazard associated with trade conditions for survival and that a pH lower than 6.0 in pork and pork products. Another review of public or higher than 8.0 inactivates leptospires. health hazards from small ruminant meat also Mitscherlich and Marth (1984) report that leptospires concluded that meat and meat products from survived 5 minutes at 55°C and survived less than 1 infected animals are not vehicles for transmission of minute at 60°C. leptospirosis to humans (Pepin et al. 1997).

Leptospira spp. are not identified as a hazard in unrestricted meat imports from the European Union.

References

Ahmed A, Engelberts MFM, Boer KR, Ahmed N Hunter P (2004). Leptospirosis. In: Infectious Diseases and Hartskeerl RA (2009). Development and o f Livestock, (eds.) JA W Coetzer, RC Tustin, Oxford validation of a real-time PCR for detection of University Press, Cape Town. pathogenic Leptospira species in clinical material, Public Library of Science One 4 (9), 1-8. Available at: Mitscherlich E and Marth EH (1984). Table 40 http://www.plosone.org/article/info%3Adoi%2F10. Culture. In: Microbial Survival in the Environment. 1371%2Fjournal.pone.0007093, last accessed 27 Springer-Verlag, Berlin. P. 588. September 2013. Pepin M, Russo P and Pardon P (1997). Public Ellis WA and Little TWA (1986). The present state of health hazards from small ruminant meat products in Leptospirosis diagnosis and control . A seminar in the CEC Europe. Revue Scientifique et Technique Office International programme o f coordination of research on animal pathology, des Lpigooties 16, 415-425. held at the Veterinary Research Laboratories, Belfast, Northern Ireland, October 10-11, 1984. Sponsored Radostits OM, Gay CC, Hinchcliff KW and by the Commission of the European Communities, Constable PD (2007). Diseases associated with Directorate-General for Agriculture, Coordination of bacteria- V. In Veterinary Medicine A Textbook of the Agricultural Research. Martinus Nijhoff Publishers, Diseases o f Cattle, Horses, Sheep, Pigs and Goats, (eds.) Kluwer Academic Publishers Group, Lancaster. OM Radostits, CC Gay, KW Hinchcliff, PD Constable, Elsevier, Edinburgh. Pp. 1094-1110. Farez S and Morley RS (1997). Potential animal health hazards of pork and pork products. Revue Reilly JR, Hanson LE and Ferris DH (1970). Scientifique et Technique Office International des Lpigooties Experimentally induced predator chain transmission 16, 65-78. of Leptospira grippotyphosa from rodents to wild marsupialia and carnivora. American Journal Veterinary Greene CE, Sykes JE, Brown CA and Hartmann Research 31, 1443-1448. K (2006). Leptospirosis. In: Infectious Diseases of the Dog and Cat, (ed.) CE Greene, Elsevier, St. Louis.

Ho HF and Blackmore DK (1979). Effect of chilling and freezing on survival of Leptospira interrogans serovarpomona in naturally infected pig kidneys. New Zealand Veterinary Journal 27, 121-123.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union World Health Organization (2003). Human Leptospirosis: Guidance for Diagnosis, Surveillance and Control, World Health Organization, Geneva. Available at: http://whqlibdoc.who.int/hq/2003/WHO CDS CS R EPH 2002.23.pdf, last accessed 27 September 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 39. MYCOBACTERIUM BOVIS

39.1. HAZARD IDENTIFICATION 39.1.1. Aetiological agent 39.1.2. Iceland status

Mycobacterium bovis is an intracellular bacterium that Bovine tuberculosis was last reported in Iceland in causes bovine tuberculosis in several species of 1959 and is listed as a group A notifiable disease in mammal, including humans. It is a member of the M. Act No 25/1993 (Willeberg 2013). Ongoing freedom tuberculosis complex (genetically similar organisms) is supported by general surveillance (OIE 2013). where M. tuberculosis is mainly a human pathogen and M. bovis principally associated with cattle (Biet et al. 2005). 39.1.3. European Union status

Table 32 (below) summarises the bovine tuberculosis status of the 28 countries of the European Union based on their official returns to the OIE.

Table 32: Status of bovine tuberculosis in European Union countries based on their official 2012 returns to the OIE (OIE 2013)

EU Member Disease status Other A ustria Present No clinical disease Belgium Present No clinical disease Bulgaria Freedom Last reported June 2008 (domestic); 2005 (wild) C roatia Present No clinical disease Cyprus Freedom Last reported 1928 Czech Republic Freedom Last reported July 2002 Denmark Freedom Last reported 1994 Estonia Freedom Last reported 1986 Finland Freedom Last reported 1982 France Present Disease restricted to certain zones Germany Freedom Last reported May 2012 (domestic); November 2009 (wild) Greece Present Disease restricted to certain zones Hungary Present Disease restricted to certain zones Ireland Present No clinical disease Italy Present Disease restricted to certain zones Latvia Freedom Last reported July 1989 Lithuania Freedom Last reported December 2010 Luxembourg Freedom Last reported 1981 Malta Freedom Last reported 2001 Netherlands Present No clinical disease Poland Present Clinical disease Portugal Present Disease limited to one or more zones R om ania Present Clinical disease Slovakia Freedom Last occurrence unknown Slovenia Freedom Last reported June 2012 Spain Present Disease restricted to certain zones Sweden Freedom Last reported January 2005 United Kingdom Present Clinical disease

39.1.4. Epidemiology pulmonary tuberculosis or from infected dust particles is the primary route of infection between animals although infection by ingestion is recognised; Mycobacterium bovis has a wide host range in addition to milk from infected cows may infect calves. cattle although infection is rare in sheep and uncommon in goats (Cousins et aL 2004). Aerosol transmission from coughing or sneezing animals with Historically, transmission to humans occurred as a result of consuming unpasteurised milk and dairy

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union products although the introduction of milk generally identified at an early stage of infection and pasteurisation has had a dramatic impact on this in cases of advanced disease with TB abscesses in the developed countries. The vast majority of human muscle and bone tissue are very rare. Furthermore, tuberculosis cases in the developed world are now carcasses containing signs of TB are completely or caused by M. tuberculosis acquired directly from an part condemned during routine meat inspection” infectious person and are not associated with M. bovis (United Kingdom Health Protection Agency 2009). (Bissielo et al. 2010). Although feeding of uncooked severely affected Following infection with M. bovis, the primary lesions carcasses to animals may introduce M. bovis into a are localised to the organ of entry and/or the naïve population, it is extremely unlikely that there associated lymph node. Usually these are within the would be a sufficient dose to achieve an infection. respiratory or alimentary system where the infection Animals dying from military tuberculosis have only remains localised and chronic with development of 100-200 bacilli present per gram of muscle tissue nodular granulomas (tubercles). Infection may whereas several million bacilli are required to achieve spread to other organs or becomes generalised infection via the oral route (Francis 1973; Cousins et causing miliary tuberculosis. The clinical signs and al. 2004). pathology vary according to which organs are infected. Furthermore, an exporting country with endemic bovine tuberculosis is likely to have testing There are few recent studies regarding meat and meat programmes that increase the likelihood that infected products as a mechanism of transmission of M. bovis. animals are identified at an early stage of infection. Francis (1973) reported that meat harbours few or no Cases of severe disease with abscesses in the muscle tubercle bacilli and that the oral infective dose is large and bone tissue are very rare in any case, but testing in comparison to the respiratory infective dose. generally enables eradication of infected animals Tuberculous meat eaten by humans poses only a very before clinical signs appear (de la Rua-Domenech slight risk of infection. This is still generally true even 2006). when cattle have quite severe lesions of tuberculosis. Although endemic countries with no control A more recent review noted that lesions involving the programme may have a higher proportion of cattle muscle mass are rare and mostly encountered only in presented for slaughter with clinical or subclinical the advanced stages of the disease at a time when disease, meat eligible for importation must be from other tissues show overt signs of tuberculosis. The animals that have met the commodity definition (see occurrence of viable M. bovis in the muscle mass of Section 4). food-producing animals infected with M. bovis is much less common than the recovery of M. bovis Meat and meat products for import must be derived from organs such as the lungs, liver, spleen, kidneys, from animals that have passed ante-mortem and and mammary gland. It was concluded that meat post-mortem inspection in slaughter and processing derived from abattoirs under the control of the plants approved for export, which operate effective competent authority presented a very low risk and Good Manufacturing Practice (GMP) and Hazard that transmission of M. bovis to humans through the Analysis and Critical Control Point (HACCP) consumption of meat had not been documented as a programmes. Under these conditions any carcasses public health concern in many countries over a containing signs of tuberculosis would be completely number of decades (Food Safety Authority of Ireland or partly condemned during routine meat inspection. 2008). 39.1.5. Hazard identification conclusion Consistent with this, the United States Food Safety and Inspection Service have stated that “tuberculosis is not transmitted by a foodborne route” (United Meat is not likely to be a source of sufficient bacilli to States Food Safety and Inspection Service 1997). achieve an infectious dose of M. bovis via the oral route. Furthermore, routine ante-mortem and post­ mortem inspection would be highly likely to identify Similarly, the United Kingdom Health Protection infected individuals at slaughter. M. bovis is not Agency concluded that “meat is highly unlikely to be identified as a hazard in unrestricted meat imports a source of infection in Great Britain, as the routine from the European Union. TB testing programme means that cattle with TB are

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union References

Biet F, Boschiroli ML, Thorel MF and Francis (1973). Very small public health risk from GuilloteauLA (2005). Zoonotic aspects of flesh of tuberculous cattle. Australian Veterinary Mycobacerium bovis and Mycobacterium avium-intracellulare Journal. 49, 496-497. complex (MAC). Veterinary Research 36, 411-436. OIE (2013). World Animal Health Information Bissielo, A, Lim E and Heffernan H (2011). Database (WAHID) Interface. Available at: Tuberculosis in New Zealand: Annual Report 2010, http://www.oie.int/wahis 2/public/wahid.php/Wah Institute of Environmental Science and Research Ltd idhome/Home, last accessed 1 July 2103. (ESR): Wellington, New Zealand. Available at: http://www.surv.esr.cri.nz/PDF surveillance/AnnT United Kingdom Health Protection Agency BRe.ports/TBAnnualRe.port2010.pdf. last accessed 30 (2009). Reducing the risk of human M bovis infection: August 2013. information for farmers. Available at: http: / / www.hpa.org.uk/webc/HPAwebFile/HPAwe Cousins DV, Huchzermeyer HFKA, Griffin JFT, b C/1259151943662 , last accessed 30 August 2013. Brueckner GK, van Rensburg IBJ and Kriek NPJ (2004). Tuberculosis. In: Infectious Diseases of Livestock, United States Food Safety and Inspection Service Edited by Coetzer JAW, Tustin RC. Oxford (1997). Tuberculosis, what you need to know. US University Press, Cape Town. Pp. 1973-1993. Department of Agriclture Food Safety and Inspection Service, Washington, DC. Available at: http: / / origin- de la Rua-Domenech R (2006). Human www.fsis.usda.gov/OPHS/tbbroch.htm , last Mycobacterium bovis infection in the United Kingdom: accessed 30 August 2013. incidence, risks, control measures and review of the zoonotic aspects of bovine tuberculosis. Tuberculosis W illeberg P (2013). Chapter 5. Notification and 86, 77-109. animal disease surveillance. In: Risk assessments regarding open trade in live animals to Iceland. Icelandic Food Safety Authority of Ireland (2008). Zoonotic Food and Veterinary Authority (MAST), Reykjavik, tuberculosis and food safety. Dublin. Available at: Iceland. Pp. 59-90. http://www.fsai.ie/uploadedFiles/Zoonotic TB.pdf , last accessed 30 August 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 40. MYCOPLASMA SPP. (OIE-LISTED)

40.1. HAZARD IDENTIFICATION 40.1.1. Aetiological agent M. synoviae was present in Iceland poultry between 1995 and 2003 and the infection is now considered to be eradicated. No seropositive samples were This Chapter addresses: detected in surveys in 2009 and 2010. M. gallisepticum has never been detected and serological surveys have • Avian mycoplasmosis (caused by either been undertaken since 1995 (Willeberg 2013). Mycoplasma synoviae or M. gallispeticiini) Ongoing freedom from M. synoviae and M. gallispeticum • Contagious agalactia (caused principally by is supported by general and targeted surveillance M. agalactiae) (OIE 2013). • Contagious bovine pleuropneumonia (caused by M. mycoides subsp. mycoides SC Contagious agalactia, contagious bovine (.Mmm SC)) pleuropneumonia, and contagious caprine • Contagious caprine pleuropneumonia pleuropneumonia have never been reported in (caused by M. capricolum subspecies Iceland. Ongoing freedom from these three diseases capripneumoniae (Mccp). is supported by general surveillance (OIE 2013).

40.1.2. Iceland status 40.1.3. European Union status

Contagious agalactia, contagious bovine Tables 33, 34, 35, 36, and 37 (below) summarise the pleuropneumonia, and contagious caprine status of the 28 countries of the European Union pleuropneumonia are listed as group A notifiable with regard to mycoplasmosis (due to M. synoviae and diseases in Act No 25/1993, avian mycoplasmosis M. gallispeticum), contagious agalactia, contagious due to M. gallisepticum or M. meleagridis is listed as a bovine pleuropneumonia, and contagious caprine group B notifiable disease and avian mycoplasmosis pleuropneumonia based on their official returns to (other than due to M. gallisepticum or M. meleagridis) is the OIE. listed as a group C disease (Willeberg 2013).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 33: Status of avian mycoplasmosis (M. synoviae) in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Not reported Belgium Present Clinical disease Bulgaria Not reported Croatia Freedom Last occurrence unknown Cyprus Freedom Last reported December 2008 Czech Republic Freedom Last reported 2003 Denmark Freedom Last occurrence unknown Estonia Freedom Last occurrence unknown Finland Freedom Last reported June 2012 France Present Disease suspected Germany Freedom Last occurrence unknown Greece Present Infection present in one or more zones Hungary Freedom Last reported December 2011 Ireland Present Clinical disease Italy Freedom Last occurrence unknown Latvia Freedom Has never occurred Lithuania Freedom Last occurrence unknown Luxembourg Freedom Has never occurred Malta Freedom Last reported 2007 Netherlands Present Clinical disease Poland Present Clinical disease Portugal Freedom Last reported December 2011 Romania Freedom Has never occurred Slovakia Freedom Last occurrence unknown Slovenia Freedom Last occurrence unknown Spain Present Clinical disease Sweden Freedom Last reported 2000 United Kingdom Present Disease restricted to certain zones

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 34: Status of avian mycoplasmosis (M. gallisepticum) in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Not reported Belgium Freedom Last reported 2011 Bulgaria Not reported Croatia Freedom Last occurrence unknown Cyprus Freedom Last reported December 2008 Czech Republic Freedom Last reported 2003 Denmark Freedom Last reported 1967 Estonia Freedom Last occurrence unknown Finland Freedom Last reported 1988 France Present Disease suspected Germany Freedom Last reported 2006 Greece Freedom Last reported December 2010 Hungary Present Disease restricted to certain zones Ireland Present Clinical disease Italy Present Infection present in one or more zones Latvia Freedom Last reported 2004 Lithuania Freedom Last occurrence unknown Luxembourg Freedom Last occurrence unknown Malta Freedom Last reported 2007 Netherlands Present Clinical disease Poland Present Clinical disease Portugal Freedom Last reported December 2011 Romania Freedom Last reported 2004 Slovakia Freedom Last reported 2001 Slovenia Freedom Last reported June 2012 Spain Present Clinical disease Sweden Present Clinical disease United Kingdom Present Clinical disease

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 35: Status of contagious agalactia in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 2000 Croatia Freedom Last occurrence unknown Cyprus Freedom Last reported December 2011 Czech Republic Freedom Last occurrence unknown Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Present Disease restricted to certain zones Germany Freedom Has never occurred Greece Present Disease restricted to certain zones Hungary Freedom Last reported 2003 Ireland Freedom Has never occurred Italy Present Disease restricted to certain zones Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Last reported 1988 Netherlands Freedom Has never occurred Poland Freedom Has never occurred Portugal Freedom Last reported December 2011 Romania Freedom Last reported 2004 Slovakia Freedom Last occurrence unknown Slovenia Freedom Has never occurred Spain Present Clinical disease Sweden Freedom Has never occurred United Kingdom Freedom Last occurrence unknown

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 36: Status of contagious bovine pleuropneumonia in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last reported 1921 Belgium Freedom Last reported 1897 Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 1902 Denmark Freedom Last reported 1886 Estonia Freedom Has never occurred Finland Freedom Last reported 1920 France Freedom Last reported 1984 Germany Freedom Last reported 1926 Greece Freedom Has never occurred Hungary Freedom Last reported 1901 Ireland Freedom Last reported 1892 Italy Freedom Last reported October 1993 Latvia Freedom Last reported 1922 Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Last reported 1887 Poland Freedom Last reported 1936 Portugal Freedom Last reported March 1999 Romania Freedom Last reported 1919 Slovakia Freedom Last reported 1902 Slovenia Freedom Has never occurred Spain Freedom Last reported April 1994 Sweden Freedom Last reported 1856 United Kingdom Freedom Last reported 1898

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 37: Status of contagious caprine pleuropneumonia in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Has never occurred Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 1902 Denmark Freedom Has never occurred Estonia Freedom Has never occurred Finland Freedom Has never occurred France Freedom Has never occurred Germany Freedom Has never occurred Greece Freedom Last reported 2006 Hungary Freedom Has never occurred Ireland Freedom Has never occurred Italy Freedom Last reported 1983 (wildlife) Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Has never occurred Malta Freedom Has never occurred Netherlands Freedom Has never occurred Poland Not reported Portugal Freedom Last reported 2002 Romania Freedom Has never occurred Slovakia Not reported Slovenia Freedom Has never occurred Spain Freedom Last occurrence unknown Sweden Freedom Last reported 1983 United Kingdom Freedom Has never occurred

40.1.4. Epidemiology affected by strain differences (Levisohn et al. 1985). However, these differences did not correlate with the pathogenicity of respiratory infection in vivo M ycoplasma ga llis e p tic u m (Levisohn et al. 1986).

M. gallisepticum has a world-wide distribution M. gallisepticum strains may also vary in tissue tropism (Levisohn and Kleven 2000) and occurs primarily in (Bradbury and Morrow 2008). Epithelial surfaces are domestic and free-ranging gallinaceous birds, the main targets, especially the trachea (Bradbury and especially chickens and turkeys (Ley 2008). Isolation Morrow 2008). However, transient systemic of M. gallisepticum from the respiratory tract of ducks infections have been described which may result in with no apparent clinical signs has been reported infection at other sites (Thomas et al. 1966; Chin et al. (Bencina et aL 1988a) and experimental infection of 1991). Variant strains of M. gallisepticum have shown specific-pathogen-free (SPF) ducks with M. predilection for other organs, including the cloaca gallisepticum resulted in colonisation but only limited (MacOwan et al. 1983) and the eye (Power and Jordan respiratory signs (Levisohn and Kleven 2000). The 1976). organism has also occasionally been recovered from other avian species including pheasants, chukar partridge, peafowl, Japanese quail (Reece et al. 1986; Birds are susceptible to M. gallisepticum at any age, Cookson and Shivaprasad 1994; Murakami et al. 2002; although clinical signs are more common in young Bencina et al. 2003), geese (Buntz et al. 1986), a birds (Bradbury and Morrow 2008). M. gallisepticum yellow-naped Amazon parrot (Bozeman et al. 1984), can have a range of clinical manifestations, but greater flamingos and white pelicans (El-Shater 1996). generally infection without complicating factors is No human health or zoonotic issues are associated mild or sub-clinical in chickens (Yagihashi and Tajima with M. gallisepticum (Levisohn and Kleven 2000). 1986; Levisohn and Kleven 2000). Respiratory signs are most common and other clinical presentations, including swelling of the hock and lameness, are rare Variability occurs both within and among strains of (Bradbury and Morrow 2008). M. gallisepticum (Bencina et al. 1994; Garcia et al. 1994) and chicken embryo mortality was found to be

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union More severe disease is associated with concurrent Given the limited tissue distribution following natural infections or environmental stressors (Kleven 1998) infection, M. synoviae is unlikely to be transmitted and M. gallisepticum is frequently present in a multi­ through international trade in fresh or frozen poultry factorial disease complex (Jordan 1972; Kleven 1998) meat products produced for human consumption causing chronic respiratory disease in chickens (Cobb 2011). (Bradbury and Morrow 2008). M ycoplasma agalactiae The incubation period varies from 6 to 21 days depending on strain virulence (Ley 2008). M. agalactiae localises in the mammary gland, joints, or Transmission of M. gallisepticum infection occurs eye conjunctiva causing disease of varying severity in vertically (in ovo) (Lin and Kleven 1982; Glisson and sheep and goats (Bergonier et al. 1997). Young Kleven 1985; Ortiz et al. 1995), and horizontally by animals are usually infected when they drink direct or indirect contact via the upper respiratory contaminated milk or colostrum. Animals may also tract or conjunctiva following exposure to aerosols or directly ingest mycoplasmas shed in other secretions droplets (Levisohn and Kleven 2000). Spread within and excretions (Center for Food Security and Public a flock occurs through close contact but fomites may Health 2009). play a role in spread between flocks (Bradbury and Morrow 2008). The initial stage of infection is often characterised by a brief febrile syndrome, which may follow M. gallisepticum can be isolated from a variety of bacteraemia, resulting in localisation of M. agalactiae to organs, usually from the respiratory or reproductive the main target organs. Mammary gland infections tract (Domermuth et aL 1967; Amin and Jordan 1978; may result intransient hypogalactia to a total abrupt MacOwan et aL 1983; Nunoya et aL 1997). agalactia. Infection of the carpal and tarsal joints may Experimentally it has been shown that more virulent present as a range of locomotor disturbances from strains can be recovered from a wide range of tissues, mild lameness to recumbency. Infection of the eye including the bursa of Fabricius, spleen, liver and may result in conjunctivitis, leading on to kidney (Varley and Jordan 1978). parenchymatous keratitis with corneal revascularisation in one or both eyes (Bergonier et al. M ycoplasma synoviae 1997).

Chickens and turkeys are considered to be the natural Shedding of mycoplasmas by an infected individual hosts of Mycoplasma synoviae (Kleven and Ferguson- usually precedes the appearance of clinical signs by Noel 2008), although the organism has also been on to ten days (Singh et al. 1974). However, described in ducks (Bencina et aL 1988a), geese maximum shedding usually occurs during the clinical (Bencina et al. 1988b), guinea fowl (Pascucci et al. stage, with the main routes of excretion being milk, 1976), pigeons (Bencina et al. 1987), Japanese quail tears, respiratory secretions or discharge, faeces, (Bencina et al. 1987), pheasants (Bradbury et al. 2001), urine, discharge from affected joints, uterovaginal and partridges (Poveda et al. 1990). secretions, and male genital secretions (DaMassa et al. 1987; Hasso et al. 1993; Zavagli 1951). Chickens usually become infected at 4 to 16 weeks old and turkeys at 10 to 24 weeks old (Sevoian et al. As well as direct horizontal transmission of from 1958), with transmission occurring via the respiratory clinically infected animals, indirect horizontal tract. Infected birds typically develop synovitis of the transmission may occur via vectors such as mites, tendon sheaths, joints, and keel bursa, which may ticks, or fleas (Nayak and Bhowmik 1990; DaMassa progress to a caseous exudate extending from tendon and Brooks 1991), via milking machines (Zavagli sheaths and joints into muscle and air sacs (Kerr and 1951; DaMassa et al. 1987; DaMassa et al. 1992; Kinde Olson 1970; Kleven and Ferguson-Noel 2008). et al. 1994; Real et al. 1994), or via other fomites such as during shearing (Bergonier et al. 1997). Airsacculitis may be seen in the respiratory form of MacDiarmid and Thompson (1997) could find no the disease (Fletcher et al. 1976; Rhoades 1987). reference to M . agalactiae in meat and concluded that Mycoplasma synoviae can be recovered from these the risk of introduction of this organism through lesions in the early stages of disease but viable imports of meat was negligible. organisms may no longer be present once chronic disease has developed. Birds remain carriers for life M ycoplasma m ycoides subsp. m y c o id e s SC (Kleven and Ferguson-Noel 2008). Following (M m m SC) experimental infection, M. synoviae can be recovered from the trachea and sinus and, although gross Contagious bovine pleuropneumonia causes lesions may be seen in other organs (liver, spleen, and significant economic losses in infected cattle kidney), the organism is only consistently recovered populations and, occasionally, water buffalo are also from these sites following intravenous inoculation affected (Thiaucourt et al. 2004; Brown 2008). (Ghazikhanian et al. 1973; Kawakubo et al. 1980). However, under natural conditions there is no

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union evidence that clinical disease occurs in species other M ycoplasma capricolum subsp. than cattle (Thiaucourt et al. 2004). Mmm SC has c a p rip n e u m o n ia e (M ccp ) been transmitted experimentally to white-tailed deer (Yedloutschnig and Dardiri 1976) but natural cases Contagious caprine pleuropneumonia (CCPP) causes have not been described in deer and they are not major economic losses in Africa, Asia and the Middle known to be involved in maintenance or transmission East. CCPP is a respiratory disease, with lesions of the disease. confined to the thoracic cavity (Center for Food Security and Public Health 2008; OIE 2009). The The disease is confined to Africa (OIE 2013) disease is highly contagious and frequently fatal, and although European and African strains of Mmm SC is transmitted during close contact by the inhalation are recognised and sporadic cases of CBPP have of respiratory droplets. In naive herds, the morbidity emerged in Europe almost 15 years after the last rate may reach 100% and the mortality rate can be as endemic case occurred in 1967 (Cheng et al. 1995). high as 80% (Center for Food Security and Public Health 2008). In cattle, the incubation period of the disease is between three weeks and four months (Thiaucourt et Mccp is very fragile and not able to survive long al . 2004; Brown 2008). Disease spreads through outside the host, up to 3 days in tropical areas and up direct contact or via droplets and transmission over to 2 weeks in temperate zones (OIE 2009). distances of up to 200 metres under favourable Moreover, as noted above (Table 37) all countries conditions are reported. CBPP is a debilitating within the European Union are free from this disease. respiratory disease and typical lesions of pleuropneumonia are seen at post-mortem. Many 40.1.5. Hazard identification conclusion animals are resistant to infection and, in an infected herd, as few as 8% may develop clinical signs (Thiaucourt et al. 2004). Infected young calves may Avian mycoplasmosis due to M. gallisepticum is develop arthritis without respiratory disease possibly recognised in the European Union. M. gallisepticum is due to colostrally derived immunity (Brown 2008; found predominantly in respiratory tissues although Thiaucourt et al. 2004). highly virulent strains may disseminate more widely. Fresh or frozen poultry meat products produced for human consumption are not ordinarily considered Recovered animals may have sequestered lesions in risks for M. gallisepticum infection (Levisohn and their lungs and may be potential carriers of infection Kleven 2000). (Thiaucourt et al. 2004; Brown 2008). Viable organisms are encapsulated and survive in these sequestra for months and up to 2 years. However, although upper respiratory tract material, reproductive tract tissues, and abdominal viscera will be removed from poultry carcases, remnants of these For meat and meat products that do not contain lung tissues may remain following automated processing tissue, Mmm SC will not be present in these so M. gallisepticum is identified as a potential hazard in commodities. In addition, the organism is fragile and imported whole poultry carcases. In contrast, under does not survive outside the animal host for more natural conditions, M. synoviae has a more limited than a few days (Brown 2008). As noted earlier, tissue distribution in an infected bird than M. natural transmission of CBPP occurs by droplet gallispeticum. Therefore, M. synoviae is not identified as infection from diseased cattle or from subclinical a hazard in imported poultry meat. carriers actively excreting Mmm SC to susceptible animals in close contact. Ingestion of infected fodder or direct exposure to diseased organs of animals There is no evidence to suggest M. agalactiae is likely clinically ill from CBPP does not transmit infection to be transmitted in meat and meat products, so this (Thiaucourt et al. 2004). organism is not identified as a hazard.

The OIE considers meat and meat products It is unlikely that M. mycoides subsp. mycoides SC or M. (excluding lung) to be safe commodities. When capricolum subsp. capripneumoniae (Mccp) would be authorising import or transit of meat and meat transmitted through imports of meat or meat products (excluding lung), the Code recommends no products and all members of the European Union are conditions related to CBPP be required regardless of free from CBPP and CCPP. Therefore, these two the CBPP status of the domestic cattle and water organisms are not identified as hazards. buffalo population of the exporting country, zone or compartment. 40.2. RISK ASSESSMENT 40.2.1. Entry assessment Furthermore, as described above (Table 36) CBPP is not currently recognised in the European Union. Mycoplasma infections are rarely associated with marked clinical signs unless accompanied by concurrent infections or environmental stressors.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Subclinically infected birds are unlikely to be detected a negligible likelihood of M. gallisepticum persisting in during ante-mortem and post-mortem inspection. scraps of poultry carcases following domestic cooking. The lack of a cell wall renders mollicutes fragile in the environment (Bradbury and Morrow 2008). They are Any respiratory or reproductive tissue remnants in readily killed by disinfectants and do not survive for imported poultry carcases would be unlikely to be prolonged periods outside the host (Bradbury and removed prior to cooking, although in the absence of Morrow 2008; Ley 2008). In one study, M. any data to support this, it is assumed that some gallisepticum persisted for 7-28 days at 4°C, 7-14 days remnants may be discarded as raw tissue prior to at room temperature, and less than 7 days at 30°C cooking and therefore accessible to backyard poultry and 37°C (Nagatomo et al. 2001). It is thought that or wild birds. mycoplasmas may be able to exist for a longer period within animal tissues (Nagatomo et al. 2001). Horizontal transmission of Mycoplasma spp. occurs Chandiramani et al. (1966) recovered M. gallisepticum either through aerosol or infectious droplet from muscle tissue of intravenously inoculated transmission resulting in localised infection of the chickens for up to 49 days at 6°C, 3 days at 20°C, and upper respiratory tract or conjunctiva, or through less than 1 day at 37°C; and from whole carcases for venereal transmission (Chin et al. 2008; Kleven and up to 4 weeks when stored under conditions varying Ferguson-Noel 2008; Ley 2008). The oral dose between 2°C and 24°C. In contrast, Peters et al. sufficient to initiate infection is not known and there (1966) demonstrated the organism in the respiratory are no field observations to support this as a natural tract, brain, kidney, and spleen from 3 to 30 days pathway (Bradbury and Kleven 2008). following intra-tracheal inoculation of turkeys but was unable to isolate the organism from skeletal Fresh or frozen poultry meat products produced for muscle. human consumption are not ordinarily considered risks for M. gallisepticum infection (Levisohn and Although experimental infections have been Kleven 2000). Goldberg et al. (1995) were unable to associated with widespread dissemination, Mycoplasma isolate any of the mycoplasmas usually associated spp. localise principally in respiratory and with clinical problems in domestic poultry from wild reproductive tissues following natural infection. As birds. noted above, remnants of these tissues may remain following automated processing. Considering the above, the likelihood of exposure for M. gallisepticum is assessed to be negligible. Considering the above, the likelihood of entry of M. gallisepticum in imported whole poultry carcases is assessed to be very low. 40.2.3. Risk estimation

40.2.2. Exposure assessment Since the exposure assessment is negligible, the risk is estimated to be negligible and Mycoplasma spp. (OIE- Listed) are not assessed to be a risk in unrestricted The growth range for a number of Mycoplasma spp. is meat imports from the European Union. described as 24°C to 42°C with rapid inactivation described at temperatures above 53°C (Mitscherlich and Marth 1984). It is therefore assessed that there is

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Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 41. MYCOPLASMA SPP. (NON OIE-LISTED AVIAN ISOLATES)

41.1. HAZARD IDENTIFICATION 41.1.1. Aetiological agent M ycoplasma cloacal is recovered commonly in wild and domestic duck species in many countries without any associated signs of disease (Goldberg et Avian Mollicutes are divided into two orders: al. 1995). Natural infections of other poultry species Mycoplasmatales (genera Mycoplasma and Ureaplasma) have not been described. and Acholeplasmatales (genus Acholeplasma) (Nicolet 1996; Stipkovits and Kempf 1996). M ycoplasma gallinaceum may be frequently isolated from a number of game bird species Mycoplasma gallinaceum, M. gallinarum, M. gallisepticum, although the pathogenic role of this organisms (if M. glycophilum, M. iners, M. iowae, M. imitans, M. any) is unknown (Bradbury et al. 2001) lipofaciens, M. pullorum, M. synoviae, and Ureaplasma gallorale have been isolated from chickens (Stipkovits and Kempf 1996; Bradbury and Morrow 2008). M ycoplasma gallinarum is found in domestic poultry, including turkeys (Jordan and Amin 1980; Bencina et al. 1987b), as well as in jungle fowl (Shah- Mycoplasma meleagridis, M. iowae, M. gallisepticum, M. Majid 1987), ducks (El Ebeedy et al. 1987), and imitans, M. gallinarum, M. pullorum, M. synoviae, and pigeons (Reece et al. 1986). M. gallinarum is generally Ureaplasma spp. have been recovered from turkeys not considered to be a pathogenic mycoplasma (Kleven 2008). although one report has linked this organism to airsaccultitis in broiler chickens (Kleven et al. 1978). Mycoplasma anatis, M. cloacale, M. gallisepticum, M. glycophilum, M. imitans, M. lipofaciens, Acholeplasma M ycoplasma glycophilum is rarely reported and axanthum, and A. laidlawii have been isolated from has not been described as a cause of disease in ducks (Goldberg et al. 1995; Stipkovits and Kempf poultry. It is not known whether M. glycophilum is 1996; Bradbury and Morrow 2008). pathogenic (Bradbury et al. 2001). However, unpublished pathogenicity studies have indicated that Avian mycoplasmosis associated with M. gallisepticum it may cause caecal enlargement and possible stunting and M. synoviae are OIE-Listed diseases and are of chickens (Forrest and Bradbury 1984; Loria et al. discussed in Chapter 40 of this document. 2008). Natural infections of chickens resulting in disease have not been described. 41.1.2. Iceland status M ycoplasma iners has been recovered from healthy Mycoplasma meleagridis has never been detected in chickens and from broilers with respiratory disease. Iceland and infections due to M. meleagridis are The pathogenic role of this organism is unknown notifiable, according to Act No 25/1993. Systematic (Tan et al. 2010). surveillance for M. meleagridis started in 2011. Other avian Mycoplasma spp. have not been reported. M ycoplasma iowae has a worldwide in distribution, including Europe (Jordan and Amin 1980; Bencina et 41.1.3. European Union status al. 1987a), India (Rathore et al. 1979), Japan (Shimizu et al. 1979), and the United States (Yoder and Hofstad 1962). Although this organisms is now rare in A wide range of Mycoplasma spp. have been recovered commercial flocks due to eradication efforts from avian species in the European Union (discussed (Bradbury and Morrow 2008), recent outbreaks have below). been recorded in commercial turkeys in the USA and Italy (Catania et al. 2012). 41.1.4. Epidemiology The natural host of M. iowae is the turkey (Bradbury M ycoplasma anati has been identified to be and Kleven 2008) and it has also been found in pathogenic to domestic and wild ducklings and eggs chickens (Yoder and Hofstad 1962; Bencina et al. and could be isolated from the respiratory tracts, 1987a), ducks (Lo et al. 1994), parrots (Bozeman et al. sinuses, and cloacae of waterfowl. Infection can 1984), geese, and wild birds including starling, cause clinical disease of the respiratory disease, cormorants, heron, wood pigeons, and a European reduced hatchability, conjunctivitis, rhinitis, sinusitis, eider (Al-Ankari and Bradbury 1996). Naturally- tenosynovitis, arthritis, and growth retardation. Co­ occurring disease is mainly restricted to turkeys with infection with Escherichia coli has been associated with occasional reports of disease in chickens (Trampel large mortalities and great economic loss for duck and Goll 1994; Al-Ankari and Bradbury 1996). farms in China (Guo et al. 2011).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union M. iowae is not associated with clinical disease in live lesions in these species (Abdul-Wahab et aL 1996; turkeys although infection is associated with a Ganapathy and Bradbury 1999). Experimental reduction in poult hatchability in the order of 2% to infection of day-old turkey poults with a partridge 5% (Bradbury and Kleven 2008) and one report has isolate of M. imitans that had been passaged through associated M. iowae with leg weakness (Trampel and turkey poults results in mild upper respiratory tract Goll 1994). Following experimental infection of one- disease, with the organism establishing in the sinuses, day-old poults, M. iowae was recovered predominantly eyes, and upper trachea (Ganapathy et a l 1998). from the oesophagus and air sacs of live birds Experimental infection of SPF ducks with M. imitans although isolations became less frequent with age and resulted in colonisation of the respiratory tract, but the organism could not be recovered from birds over no pathogenic effects were reported (Levisohn and 12 weeks (Bradbury et aL 1988). M. iowae has also Kleven 2000). been recovered from the semen and phallus of sexually mature toms (Shah-Majid and Rosendal M. imitans has been shown to share many phenotypic 1986) and from the oviduct of chickens (Yoder and and genotypic properties with M. gallisepticum and like Hofstad 1962; Rathore et aL 1979). M. gallisepticum it has the potential to act synergistically with respiratory viruses to exacerbate disease in Experimentally M. iowae can cause mortality in chickens (Abdul-Wahab et al. 1996). chicken embryos, as well as stunting, poor feathering, leg abnormalities, and airsacculitis in chickens M ycoplasma lipofacient has been isolated from the (Bradbury and Kleven 2008). Few reports describe respiratory tract of healthy chickens, turkeys, and these clinical signs in chickens under field ducks (Priante et al. 2011, Bradbury et al. 1983, circumstances (Bradbury and Kleven 2008). There Bencina et al. 1987b) and is believed to be a are no reports of disease caused by M. iowae in free- commensal organism. Experimental infection has ranging or commercial ducks. caused some chicken and turkey embryo mortality (Lierz 2009, Bradbury et al. 1983). There are no Transmission of M. iowae is predominantly vertical (in reports of natural infections causing disease in ovo). Horizontal transmission can also occur although poultry. the organism does not spread rapidly (Bradbury and M. lipofaciens has been isolated from the nares of a Kleven 2008). Repeated oral challenge of turkey veterinarian reporting throat pain, rhinitis and nasal poults with high dose M. iowae failed to induce clinical pain (Lierz et aL 2008). Cross-reactivity to other signs, but persistent shedding of the organism was Mycoplasma spp. cannot be excluded although there observed in most birds, and at necropsy M. iowae was remains a possibility that M. lipofaciens can be recovered from tissues of the respiratory tract, transmitted to humans and may cause clinical gastrointestinal tract, spleen, and kidney (Shah-Majid symptoms (Lierz et aL 2008). and Rosendal 1987). In the mature bird the oviduct, semen, cloaca, and faeces are sources of infection (Mirsalimi et al. 1989; Bradbury and Kleven 2008) and M ycoplasma m eleagridis is a common pathogen of M. iowae has been shown to survive in the turkeys found worldwide including Australia (Grimes gastrointestinal tract for at least 3 weeks (Shah-Majid 1972; Rosenfeld and Grimes 1972), Canada (Bigland and Rosendal 1987). Little is known about the and Benson 1968; Bigland 1969), Guatemala (Mátzer natural route of infection in chickens (Al-Ankari and Ovalle 1972), Japan (Shimizu and Yagihashi 1980), Bradbury 1996). M. iowae has only been isolated from the United Kingdom (Wise et aL 1973), and the the respiratory tract, oviduct, and hock joint of United States (Adler et al 1958), although efforts over naturally infected chickens (Yoder and Hofstad 1962; the last twenty years have significantly reduced the Rathore et al. 1979; Al-Ankari and Bradbury 1996). prevalence of M. meleagridis in the major turkey- producing areas of the world (Chin et al 2008). M. iowae has been shown to survive for 5 days or more on feathers and at least 6 days on human hair, M. meleagridis is only pathogenic in turkeys. Chickens cotton, rubber, and straw (Christensen et aL 1994). have been shown to be refractory to infection (Adler M. iowae appears to be slightly hardier in 1958; Yamamoto and Bigland 1964; Yamamoto et al environmental conditions than other mycoplasmas 1965). M. meleagridis has been isolated from healthy although the organism appears to be inactivated by free-ranging birds of prey in Germany (Lierz et al. proper cleaning and disinfection. 2000) and serological surveys have found evidence of infection in lesser prairie-chickens in Kansas (Hagen et al. 2002) and in a peafowl in Michigan (Hollamby et M ycoplasma imitans has been isolated from al. 2003). chickens, ducks, geese, and partridges (Ganapathy and Bradbury 1999) but its clinical significance has not yet been established (Levisohn and Kleven 2000). M. meleagridis spreads vertically, with hens being infected during their embryonic development. Insemination with mycoplasma-contaminated semen Natural infection of chicken, turkeys, or ducks has also plays a major role in sustaining the egg- not been described and it is known that M. imitans transmission rate during the laying season (Kumar alone does not produce any clinical signs or gross

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union and Pomeroy 1969; Yamamoto and Ortmayer 1969; pathogen-free turkey flock in France that was able to Kleven and Pomeroy 1971; Matzer and Yamamoto induce embryonic mortality when experimentally 1974). Horizontal transmission of M. meleagridis has inoculated into chicken and turkey eggs (Moalic et al. been described in a hatchery (Kumar and Pomeroy 1997). Naturally-occurring disease in poultry due to 1969), flock (Yamamoto and Ortmayer 1967), or M. pullorum has not been described. between flocks (Yan Ghazikhanian et aL 1980). Infection due to horizontal transmission usually Ureaplasma spp. have been recovered from healthy results in localised infections of the sinus and trachea poultry on a number of occasions (Harasawa et al. (Mohamed and Bohl 1967; Yamamoto and Ortmayer 1985; Koshimizu et al. 1987; Priante et al. 2011) and 1967; Kumar and Pomeroy 1969). very little is known about their spread and pathogenicity (Stipkovits and Kempf 1996). Infection of poults with M. meleagridis causes Experimental studies have had mixed results. In one airsaccultitis, which is rarely accompanied by clinical study inoculation failed to produce clinical signs or signs. M. meleagridis has no effect on egg production macroscopic lesions (Koshimizu et al. 1982) and in or fertility although it has been associated with late another, inoculation produced mild upper respiratory incubation mortality in naturally infected turkey clinical signs with a serofibrinous airsacculitis and embryos, and has been estimated to produce a 5-6% peritonitis (Stipkovits et al. 1978). An investigation of loss of fertile eggs. Airsacculitis may result in carcase infertility in a turkey-breeding farm in Eastern condemnations at slaughter, especially where co­ Europe was associated with the presence of infections or exacerbating environmental factors are Ureaplasma spp. in tom semen (Stipkovits et al. 1983). present. M. meleagridis may also adversely affect There are no reports of naturally-occurring disease weight gain in infected poults (Chin et aL 2008). caused by Ureaplasma spp. in commercial poultry.

Airsacculitis deficiency syndrome (also known as 41.1.5. Hazard identification conclusion Turkey Y disease or Turkey syndrome ’65) is characterised by stunting, poor feathering, and leg M. cloacale, M. gallinaceum, M. gallinarum, M. glycophilum, bone abnormalities and has been associated with M. M. imitans, M. iners, M. lipofaciens, M. pullorum, and meleagridis (Gordon et aL 1965, Wise et aL 1973). Ureaplasma spp. have been isolated from healthy However, this syndrome has also been reproduced poultry and there is little evidence to suggest that they using M. gallisepticum isolates (Wannop and Butler have a pathogenic role in natural infections. Where 1968; Wannop et al. 1971) and is likely to be due to a experimental infections have resulted in clinical combination of nutritional factors alongside disease, the organisms are confined to the upper mycoplasmal infections (Grasso 1968; Wannop et al. respiratory tract tissues. 1971; Wise et al. 1973). These organisms are not identified as hazards. M. meleagridis may also act synergistically with other M. anatis has been associated with respiratory disease mycoplasma isolates to produce a severe form of in ducks, although following infection this organism airsaccultitis (Rhoades 1981) and M. meleagridis has has a limited tissue distribution (respiratory tracts, been shown to act synergistically with M. synoviae to sinuses, and cloacae). produce synovitis in experimentally infected turkeys (Rhoades 1977). M. iowae is recognised as a pathogen of turkeys and chickens, although following infection this organism also has a limited tissue distribution (upper A study of 300 naturally-infected turkey embryos respiratory tract, reproductive organs, and hock demonstrated that M. meleagridis localises to the joint). respiratory tissues, with the organism detected in the sinus, peritoneum, lung, trachea and air sacs (Bigland M. meleagridis is a pathogen of turkeys and localises 1972) and experimental infection of embryos has predominantly in the tissues of the respiratory tract. shown that the organism also localises to the intestine and bursa of Fabricius (Reis and Yamamoto 1971). M. anatis is identified as a potential hazard in Although gross lesions in natural infections are imported entire duck carcases, M. iowae and M. limited to the air sacs (Chin et al. 2008), experimental meleagridis are identified as potential hazards in infections using M. meleagridis have been associated imported entire turkey carcases, and M. iowae is with sternal bursitis (Yamamoto and Bigland 1965), identified as a potential hazard in imported entire synovitis (Saif et al. 1970), and ascites (Wise and chicken carcases. Fuller 1975). 41.2. RISK ASSESSMENT M ycoplasma pullorum is frequently isolated from 41.2.1. Entry assessment healthy birds, including chickens, quail, partridge, pheasants, turkeys, and ducks (Lo et al. 1994; Kleven Mycoplasma infections are rarely associated with and Ferguson-Noel 2008) and the organism is not marked clinical signs unless accompanied by considered to be pathogenic (Poveda et al. 1990). An concurrent infections or environmental stressors. isolate of M. pullorum was recovered from a specific-

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Subclinically infected birds are unlikely to be detected removed prior to cooking, although in the absence of during ante-mortem and post-mortem inspection. any data to support this, it is assumed that some remnants may be discarded as raw tissue prior to The lack of a cell wall renders mollicutes fragile in the cooking and therefore accessible to backyard poultry environment. They are readily killed by disinfectants or wild birds. and do not survive for prolonged periods outside the host (Bradbury and Morrow 2008). Mycoplasma spp. Horizontal transmission of Mycoplasma spp. occurs localise principally in respiratory and reproductive either through aerosol or infectious droplet tissues following natural infection and remnants of transmission resulting in localised infection of the these tissues may remain following automated upper respiratory tract or conjunctiva, or through processing. venereal transmission (Chin et al. 2008; Kleven and Ferguson-Noel 2008). The oral dose sufficient to Considering the above, the likelihood of entry of M. initiate infection is not known and there are no field anatis, M. iowae, and M. meleagridis in imported whole observations to support this as a natural pathway poultry carcases is assessed to be very low. (Bradbury and Kleven 2008).

41.2.2. Exposure assessment Considering the above, the likelihood of exposure for M. anatis, M. iowae, or M. meleagridis is assessed to be negligible. The growth range for a number of Mycoplasma spp. is described as 24°C to 42°C with rapid inactivation described at temperatures above 53°C (Mitscherlich 41.2.3. Risk estimation and Marth 1984). It is therefore assessed that there is a negligible likelihood of M. anatis, M. iowae, or M. Since the likelihood of exposure is negligible, the risk meleagridis persisting in scraps of poultry carcases is estimated to be negligible and Mycoplasma spp. (non following domestic cooking. OIE-Listed avian isolates) are not assessed to be a risk in unrestricted meat imports from the European Any respiratory or reproductive tissue remnants in Union. imported poultry carcases would be unlikely to be

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Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Rosenfeld LE and Grimes TM (1972). Natural Wannop CC and Butler EL (1968). Turkey and experimental cases of airsacculitis associated with syndrome ’65. Veterinary Record 82, 332. Mycoplasma meleagridis infection. Australian Veterinary Journal 48, 240-243. Wannop CC, Butler EL and Pearson AW (1971). Experimental reproduction of turkey syndrome ’65 Saif YM, Moorhead PD and Bohl EH (1970). by infection with M. gallisepticum. Veterinary Record 88, Mycoplasma meleagridis and Escherichia coli infections in 30-33. germfree and specific-pathogen-free turkey poults: Production of complicated airsacculitis. American Wise DR, Boldero MK and Thornton GA (1973). Journal o f Veterinary Research 31, 1637-1643. The pathology and aetiology of turkey syndrome ’65 (T.S. 65). Research in Veterinary Science 14, 194-200. Shah-Majid M and Rosendal S (1986). Mycoplasma iowae from turkey phallus and semen. Veterinary Record Wise DR and Fuller MK (1975). Experimental 118, 435. reproduction of turkey syndrome ’65 with Mycoplasma meleagridis and M. gallisepticum and associated changes Shah-Majid M (1987). A case-control study of in serum protein characteristics. Research in Veterinary Mycoplasma gallinarum in the male and female Science 19, 201-203. reproductive tract of indigenous fowl. Israel Journal of Medical Sciences 23, 530. Yamamoto R and Bigland CH (1964). Pathogenicity to chicks of Mycoplasma associated with Shah-Majid M and Rosendal S (1987). Oral turkey airsacculitis. Avian Diseases 8, 523-531. challenge of turkey poults with Mycoplasma iowae. Avian Diseases 31, 365-369. Yamamoto R and Bigland CH (1965). Experimental production of airsacculitis in turkey Shimizu T, Numano K and Uchida K (1979). poults by inoculation with “N”-type Mycoplasma. Isolation and identification of mycoplasmas from Avian Diseases 9, 108-118. various birds: an ecological study. Japanese Journal of Veterinary Science 41, 273-282. Yamamoto R and Ortmayer HB (1967). Hatcher and intraflock transmission of Mycoplasma meleagridis. Shimizu T and Yagihashi T (1980). Isolation of Avian Diseases 11, 288-295. Mycoplasma meleagridis from turkeys in Japan. Japanese Journal o f Veterinary Science 42, 41-47. Yamamoto R and Ortmayer HB (1969). Egg transmission of Mycoplasma meleagridis in naturally Stipkovits L, Rashwan A and Sabry MZ (1978). infected turkeys under different mating systems. Studies of pathogenicity of turkey ureaplasma. Avian Poultry Science 48, 1893. Pathology 7, 577-582. Yamamoto R, Bigland CH and Ortmayer HB Stipkovits L, Brown PA, Glavits R and Julian RJ (1965). Characteristics of Mycoplasma meleagridis sp. (1983). The possible role of ureaplasma in a n., isolated from turkeys. Journal o f Bacteriology 90, 47­ continuous infertility problem in turkeys. Avian 49. Diseases 27, 513-523. Yan Gazikhanian G, Yamamoto R, McCapes Stipkovits L and Kempf I (1996). Mycoplasmoses RH, Dungan WM and Ortmayer HB (1980). in poultry. Revue Scientifique et Technique Office Combination dip and injection of turkey eggs with International des Épigooties 15, 1495-1525. antibiotics to eliminate Mycoplasma meleagridis infection from a primary breeding stock. Avian Diseases 24, 57­ Tan LJ, Dahlia H, Zarrahimah Z, 70. Chandrawathani P and Ramlan M (2010). Isolation of Mycoplasma iners from chickens. Yoder Jr HW and Hofstad MS (1962). A Malaysian Journal of Veterinary Research 1, 23-26. previously unreported serotype of avian mycoplasma. Avian Diseases 6, 147-160. Trampel DW and Goll Jr F (1994). Outbreak of Mycoplasma iowae infection in commercial turkey poults. Avian Diseases 38, 905-909.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 42. PASTEURELLA MULTOCIDA

42.1. HAZARD IDENTIFICATION 42.1.1. Aetiological agent 42.1.2. Iceland status

Haemorrhagic septicaemia is caused by Pasteurella Haemorrhagic septicaemia has never been reported in multocida, a Gram-negative coccobacillus. The Asian Iceland. Pasteurellosis is listed as a group C serotype B:2 and the African serotype E:2 (Carter and notifiable disease in Act No 25/1993 (Willeberg Heddleston system), corresponding to 6:B and 6:E 2013). Ongoing freedom is supported by general (Namioka-carter system), are mainly responsible for surveillance (OIE 2013). the disease. In wild ruminants, serotype B:2,5 is predominantly present while serotype B:3,4 also has been reported from fallow deer. The association of 42.1.3. European Union status other serotypes, namely A:1, A:3 with a similar condition in cattle and buffaloes in India has been Table 38 (below) summarises the haemorrhagic recorded (Singh 2012). septicaemia status of the 28 countries of the European Union based on their official returns to the OIE. Table 38: Status of haemorrhagic septicaemia in European Union countries based on their official returns to the OIE (OIE 2013)

EU Member Disease status Other Austria Freedom Last occurrence unknown Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 1994 Croatia Freedom Last occurrence unknown Cyprus Freedom Has never occurred Czech Republic Freedom Last occurrence unknown Denmark Freedom Has never occurred Estonia Freedom Last reported 1994 Finland Freedom Last occurrence unknown France Freedom Has never occurred Germany Freedom Last reported 1986 Greece Freedom Last reported 1993 Hungary Freedom Last reported 1970 Ireland Freedom Last occurrence unknown Italy Freedom Last reported June 2007 Latvia Present Clinical disease Lithuania Freedom Last occurrence unknown Luxembourg Freedom Last occurrence unknown Malta Freedom Last reported 2001 Netherlands Freedom Has never occurred Poland Freedom Last reported 2001 Portugal Freedom Last occurrence unknown Romania Freedom Last reported 2004 Slovakia Freedom Last occurrence unknown Slovenia Freedom Has never occurred Spain Freedom Last occurrence unknown Sweden Freedom Has never occurred United Kingdom Freedom Has never occurred

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 42.1.4. Epidemiology The incubation period varies from 3 to 5 days. In peracute cases, sudden death without clinical signs may be observed. At post mortem most animals Haemorrhagic septicaemia (HS) is an acute, highly succumbing to haemorrhagic septicaemia show fatal bacterial septicaemia of cattle and buffaloes marked swelling of the neck caused by severe blood- caused by Pasteurella multocida serotype B or E. The tinged oedema. Gross lesions are similar to those disease occurs almost exclusively in Asia (serotype B) seen in cases of severe sepsis, such as abundant and Africa (serotype E), in countries with a high and petechial haemorrhages in many tissues and organs, seasonal rainfall (Bastianello and Henton 2004). The particularly in serosal membranes (Singh 2012). recording of this disease in Latvia (Table 38) may therefore be inaccurate. 42.1.5. Hazard identification conclusion Pasteurella multocida is normally maintained as a commensal in the oropharynx of mammals (Timoney Few animals survive haemorrhagic septicaemia and et al. 1988), and various stresses (especially the sudden affected individuals show marked gross lesions typical onset of the rainy season, with an associated drop in of septicaemia. As noted above (Section 4), the temperature) are associated with disease outbreaks commodity considered here is chilled or frozen meat (Bastianello and Henton 2004). Pasteurella multocida is and meat products derived from animals that have described as a commensal of the upper respiratory passed ante-mortem and post-mortem inspection in tract or as a primary or secondary pathogen slaughter and processing plants approved for export, (Anonymous 2004). which operate effective Good Manufacturing Practice (GMP) and Hazard Analysis and Critical Control Haemorrhagic septicaemia of cattle and buffaloes is Point (HACCP) programmes. Therefore, Pasteurella characterised by an acute, highly fatal septicaemia multocida is not identified as a hazard in unrestricted with high morbidity and mortality. Septicaemia is the meat imports from the European Union. main characteristic feature in all forms of the disease.

References

Anonymous (2004). Pasteurella and Mannheimia spp. Singh VP (2012). Chapter 2.4.12. Haemorrhagic In: Coetzer JAW , Tustin RC (eds). Infectious Diseases of septicaemia. In: OIE Manual of Diagnostic Tests and Livestock. Second Edition, Volume 3. Oxford Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: University Press Southern Africa, Capetown. http: //www.oie.int/fileadmin/Home/eng/Health st Pp.1672-1676. andards/tahm/2.04.12 HAEMORRHAGIC SEPTI CAEMIA.pdf, last accessed 1 July 2013. Bastianello SS and Henton MM (2004). Haemorrhagic septicaemia. In: Coetzer JAW, Tustin Timoney JF, Gillespie JH , Scott FW and RC (eds). Infectious Diseases o f Livestock.. Second Barlough JE (1988). Hagan and Brunner’s Microbiology Edition, Volume 3. Oxford University Press and Infectious Diseases of Domestic Animals. Eighth Southern Africa, Capetown. Pp.1689-1694. Edition, Cornell University Press. Pp.106.

OIE (2013). World Animal Health Information W illeberg P (2013). Chapter 5. Notification and Database (WAHID) Interface. Available at: animal disease surveillance. In: Risk assessments http: / /www.oie.int/wahis 2/public/wahid.php/Wah regarding open trade in live animals to Iceland. Icelandic idhome/Home, last accessed 1 July 2103. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 43. SALMONELLA ABORTUS OVIS

43.1. HAZARD IDENTIFICATION 43.1.1. Aetiological agent 43.1.2. Iceland status

This disease is caused by Salmonella enterica subspecies Salmonellosis due to S. abortus ovis has never been enterica serovar (serotype) abortus ovis. Salmonella abortus reported in Iceland and is listed as a group A ovis, a member of the Enterobacteriaceae, is a short, notifiable disease in Act No 25/1993 (Willeberg aerobic, Gram-negative rod (Center for Food 2013). Ongoing freedom is supported by general Security and Public Health 2005). surveillance (OIE 2013).

43.1.3. European Union status

Table 39 (below) summarises the salmonellosis status of the 28 countries of the European Union based on their official returns to the OIE.

Table 39: Status of salmonellosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Not reported Croatia Freedom Last reported March 2010 Cyprus Freedom Last reported 1964 Czech Republic Freedom Last occurrence unknown Denmark Freedom Has never occurred Estonia Freedom Last occurrence unknown Finland Freedom Has never occurred France Present Clinical disease Germany Freedom Last reported December 2011 Greece Freedom Last occurrence unknown Hungary Freedom Last reported 1970 Ireland Not reported Italy Present Clinical disease Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Last occurrence unknown Malta Freedom Last occurrence unknown Netherlands Freedom Has never occurred Poland Not reported Portugal Freedom Last reported 2006 R om ania Present Clinical disease Slovakia Freedom Last reported June 2010 Slovenia Freedom Last occurrence unknown Spain Present Disease restricted to certain zones Sweden Freedom Has never occurred United Kingdom Present Disease restricted to certain zones

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 43.1.4. Epidemiology Salmonella abortus ovis can be found in vaginal discharges, the placenta, aborted foetuses, and infected newborns. Vaginal discharges are highly Salmonella abortus ovis is host specific for sheep infectious during the first week after an abortion and (Linklater 1983). The organism was formerly of may remain infectious for up to a month. The major importance as a pathogen in sheep in England organisms may also be recovered from the faeces of but by 1983 it was rarely diagnosed (Linklater 1983) septicaemic individuals and, more rarely, it can be and in a report written in 1983 it was stated that no found in colostrum or milk (Center for Food Security isolations of S. abortus ovis had been made since 1976 and Public Health 2005). (Sojka et al. 1983), suggesting that S. abortus ovis is no longer a common disease of sheep. Salmonella abortus ovis is almost always introduced into a flock by infected sheep and (unlike other Salmonella Following infection, the main clinical sign is abortion, species) spread by feed, water, other mammals, or usually during the second half or last third of birds is negligible (Center for Food Security and gestation. Lambs may also be stillborn or die within Public Health 2005). Although almost all feeds may a few hours of birth from septicaemia. Occasionally, act as a source of introduction of salmonellae that are lambs appear to be healthy but die within 3 weeks; not highly host-adapted, S. abortus ovis is not a food some have diarrhea or respiratory signs. During an borne pathogen. It is highly improbable that S. outbreak in a naïve flock, up to 60% of all ewes may abortus ovis would be introduced through imported abort and mortality in ewes and newborn lambs may meat or meat products (MacDiarmid and Thompson be significant. Once endemic, abortions are usually 1997). sporadic with only young animals and newly introduced sheep affected. Most ewes develop immunity after infection but some may become 43.1.5. Hazard identification conclusion carriers (Center for Food Security and Public Health 2005). Reflecting the above, S. abortus ovis is not identified as a hazard in unrestricted meat imports from the European Union. References

Center for food security and public health (2005). OIE (2013). World Animal Health Information Salmonella abortusovis. Available at: Database (WAHID) Interface. Available at: http://www.cfsph.iastate.edu/Factsheets/pdfs/salm http://www.oie.int/wahis 2/public/wahid.php/Wah onella abortusovis.pdf, last accessed 30 August 2013. idhome/Home, last accessed 1 July 2103.

Linklater KA (1983). Salmonellosis and Salmonella Sojka WJ, Wray C, Shreeve JE and Bell JC (1983). abortion. In Martin, W, ed, Diseases of sheep. The incidence of salmonella infection in sheep in Blackwell Scientific Publications, Oxford, London, England and Wales, 1975-1981. British Veterinary Edinburgh, Boston, Melbourne. Journal 139, 386-392.

MacDiarmid SC and Thompson EJ (1997). The W illeberg P (2013). Chapter 5. Notification and potential risks to animal health from imported sheep animal disease surveillance. In: Risk assessments and goat meat. In: Revue Scientifique et Technique Office regarding open trade in live animals to Iceland. Icelandic International des Épigooties 16, 45-56. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 44. SALMONELLA GALLINARUM-PULLORUM

44.1. HAZARD IDENTIFICATION 44.1.1. Aetiological agent 44.1.2. Iceland status

Salmonella Pullorum, the causal agent of pullorum Fowl typhoid was last reported in Iceland in 1953 and disease, and Salmonella Gallinarum, the causal agent of pullorum disease was last reported in Iceland in 1958. fowl typhoid. These two bacteria are currently placed Both fowl typhoid and pullorum disease are listed as in a single species, Salmonella enterica subsp. enterica a group A notifiable diseases in Act No 25/1993 serovar Gallinarum-Pullorum, hereafter referred to as (Willeberg 2013). Ongoing freedom is supported by S. Gallinarum-Pullorum (Shivaprasad and Barrow general surveillance (OIE 2013). 2008). 44.1.3. European Union status

Tables 40 and 41 (below) summarise the fowl typhoid and pullorum disease status of the 28 countries of the European Union based on their official returns to the OIE.

Table 40: Status of fowl typhoid in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last reported 2006 Bulgaria Freedom Last reported March 2006 Croatia Freedom Last reported 2006 Cyprus Freedom Last reported 2004 Czech Republic Freedom Last reported 2003 Denmark Freedom Last reported 2002 Estonia Freedom Last occurrence unknown Finland Freedom Has never occurred France Freedom Last reported 2005 Germany Freedom Last occurrence unknown Greece Freedom Last occurrence unknown Hungary Present Disease restricted to certain zones Ireland Freedom Last occurrence unknown Italy Freedom Last reported June 2011 Latvia Freedom Last reported April 1995 Lithuania Freedom Last occurrence unknown Luxembourg Freedom Last occurrence unknown Malta Freedom Last occurrence unknown Netherlands Freedom Last reported 2008 Poland Present Clinical disease Portugal Freedom Last reported 1994 Romania Freedom Last reported November 2011 Slovakia Freedom Last occurrence unknown Slovenia Freedom Last reported 1996 Spain Freedom Last reported 1991 Sweden Present Clinical disease United Kingdom Present Disease restricted to certain zones

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 41: Status of pullorum disease in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 2004 Croatia Freedom Last reported 2006 Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 2009 Denmark Freedom Last reported March 2010 Estonia Freedom Last reported 1977 Finland Freedom Last reported 1962 France Freedom Last reported November 2011 Germany Freedom Last reported 2008 Greece Present No clinical disease Hungary Freedom Last reported June 2008 Ireland Freedom Last occurrence unknown Italy Freedom Last reported 2007 (wild) Latvia Freedom Last reported April 1994 Lithuania Freedom Last occurrence unknown Luxembourg Freedom Last occurrence unknown Malta Freedom Last occurrence unknown Netherlands Freedom Last reported 2011 Poland Freedom Last reported February 2011 Portugal Freedom Last reported 1994 Romania Freedom Last reported 2004 Slovakia Freedom Last reported 2000 Slovenia Freedom Last occurrence unknown Spain Not reported Sweden Freedom Last reported 2001 United Kingdom Present Clinical disease

44.1.4. Epidemiology a flock and personnel movements, wild birds, mammals, and flies have been implicated in spread of these diseases (Shivaprasad and Barrow 2008). Chickens are the natural host for S. Gallinarum- Pullorum (Shivaprasad and Barrow 2008). S. Gallinarum-Pullorum in chickens is considered to Chickens hatched from infected eggs may be found have a worldwide distribution, including Europe moribund or dead in the incubator or shortly after (Christensen et aL 1994; Hoop and Albicker- hatching. Mortality usually peaks after 2 to 3 weeks, Rippinger 1997; Cobb et aL 2005). Pullorum disease and is accompanied by signs of huddling, laboured and fowl typhoid are rare in modern commercial breathing, poor development, blindness, and poultry companies although epizootics do still occur synovitis (Johnson et aL 1992; Salem et aL 1992; (Johnson et al. 1992; Salem et al. 1992). Mayahi et al. 1995; Shivaprasad and Barrow 2008). Infection of older chickens may not be detected but can result in acute disease outbreaks characterised by Mortality from pullorum disease usually occurs in the egg drop, diarrhoea, pyrexia, depression, dehydration, first 2-3 weeks of life although a proportion of and death which are followed by intermittent individuals become chronic carriers (Berchieri et al. recurrence and less severe losses. Losses due to 2001). Fowl typhoid tends to cause disease in older pullorum disease are reported to vary from 0 to 100% chickens although high mortality in young chicks as a whilst fowl typhoid is associated with losses from 10 result of fowl typhoid has been described historically to 93% (Cobb et al. 2005; Shivaprasad and Barrow (Beaudette 1925; Beach and Davis 1927; Martinaglia 2008). 1929; Komarov 1932).

Pullorum disease and fowl typhoid are systemic Both horizontal and vertical transmission are infections and S. Gallinarum-Pullorum can be important in the spread of S. Gallinarum-Pullorum. recovered from most internal organs of infected Transmission by contact with infected chicks in the chickens, including the liver, spleen, caeca, lungs, hatchery can disseminate infection and cannibalism heart, ventriculus, pancreas, yolk sac, synovial fluid, can contribute to spread. Contaminated feed, water, and reproductive organs (Shivaprasad and Barrow and litter may introduce S. Gallinarum-Pullorum into

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 2008). Recovery of the organism from muscle tissue 44.2. RISK ASSESSMENT following natural infection has not been documented 44.2.1. Entry assessment and chicken meat contamination with S. Gallinarum- Pullorum has only been described in environments with poor hygiene practices (Maharjan et al. 2006). The OIE Code contains measures against S. Gallinarum-Pullorum applicable to trade in live poultry and hatching eggs but not for chicken meat. In experimental studies, ducks have been shown to be resistant to infection. Buchholz and Fairbrother Wigley et al. (2001) infected one-week old chickens (1992) attempted to determine an LD 50 for S. Gallinarum-Pullorum in mallard ducks using oral orally with 109 organisms and reported that they were inoculation doses of up to 0.4x1010CFU. However, able to recover S. Gallinarum-Pullorum from breast no ducks showed any clinical signs of illness during meat only by enrichment culture during the first week this study and the authors concluded that they after infection but not subsequently, although the underwent only a short subclinical infection that was organism was found to persist in bone marrow for at resolved without any lasting tissue damage. Similarly, least 5 weeks. Furthermore, Georgiev et al. (1978) Barrow et al. (1999) concluded that S. Gallinarum- reported that S. Gallinarum-Pullorum could persist Pullorum was totally avirulent for commercial ducks on frozen poultry for at least 6 months at -18°C. when administered by the oral route. In contrast to paratyphoid Salmonella spp. which No recent reports of natural infection of commercial colonise the alimentary tract and are frequently turkeys with S. Gallinarum-Pullorum have been described as contaminants of chicken meat, found. Brant (1998) commented that pullorum contamination with S. Gallinarum-Pullorum has only disease was a major problem as the young turkey been described in environments with poor hygiene industry grew but subsequent measures in a number practices. Maharjan et al. (2006) described the of countries have virtually eliminated the disease. recovery of S. Gallinarum-Pullorum from 9% of poultry meat samples taken from a local meat market in Kathmandu and it was noted that Maharjan and There is a difference of opinion among investigators Sharma (2000) also found that 85.6% of water concerning the susceptibility of other avian species to sources in Nepal were positive for faecal S. Gallinarum-Pullorum (Buchholz and Fairbrother contamination and 10.8% of these were found to 1992). Pullorum disease has been described in contain Salmonella spp. Similarly, Soomro et al. (2010) pheasants (Pennycott and Duncan 1999) and recovered S. Gallinarum-Pullorum from poultry meat (experimentally) in bobwhite quail (Buchholz and samples collected at Hyderabad market in Pakistan Fairbrother 1992). and noted that a lack of disease control programmes associated with poor handling of raw material from There is a single reported outbreak of gastroenteritis production to marketing was a major problem in that affecting 423 people that was suggested to have been country. caused by S. Gallinarum-Pullorum contamination of eggs used in a rice pudding (Mitchell et al. 1946) and a Studies of poultry meat in a number of more subsequent experimental study found that feeding developed countries including Korea (Chung et al. humans with this organism could induce illness 2003), Poland (Mikoajczyk and Radkowski 2002), (nausea, vomiting, and diarrhoea) although this was Thailand (Padungtod and Kaneene 2006), Northern only achieved with very high dosages ranging from Ireland (Wilson 2002), Mexico (Zaidi et al. 2006), 1.3x109 to 10x109 organisms (McCullough and Eisele Belgium (Ghafir et al. 2005), and Spain (Capita et al. 1951). S. Gallinarum-Pullorum was recovered for up 2003) have consistently failed to identify S. to 121 days after infection from the faeces of rats Gallinarum-Pullorum as a contaminant of chicken orally infected with 5x108 organisms, although no meat. clinical disease was noted (Badi et al. 1992).

The commodity considered here will have passed 44.1.5. Hazard identification conclusion ante-mortem and post-mortem inspection in slaughter and processing plants which operate Chickens are recognised as the natural host of S. effective Good Manufacturing Practice (GMP) and Gallinarum-Pullorum. S. Gallinarum-Pullorum is Hazard Analysis and Critical Control Point (HACCP) identified as a potential hazard in chicken meat and programmes. Chicken meat derived from such birds meat products. is considered unlikely to act as a vehicle for the spread of S. Gallinarum-Pullorum (Cobb 2011). The Ducks have been shown to be resistant to infection likelihood of entry is therefore assessed to be with S. Gallinarum-Pullorum. S. Gallinarum- negligible. Pullorum is not identified as a hazard in duck meat or meat products. Similarly, S. Gallinarum-Pullorum is not identified as a hazard in turkey meat or meat products.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 44.2.2. Risk estimation

Since the likelihood of entry is negligible, the risk is estimated to be negligible and S. Gallinarum- Pullorum is not assessed to be a risk in unrestricted meat imports from the European Union.

References

Badi MA, Iliadis N and Sarris K (1992). Chung YH, Kim SY and Chang YH (2003). Natürliche und experimentelle infektion von Prevalence and antibiotic susceptibility of Salmonella nagetieren (Rattus norvegicus) mit Salmonella gallinarum. isolated from foods in Korea from 1993 to 2001. Berliner und Munchener Tierarytliche Wochenschrift 105, Journal of Food Protection 66, 1154-1157. 264-267. Cobb SP (2011). The spread of pathogens through Barrow PA, Lovell MA, Murphy CK and Page K trade in poultry meat: overview and recent (1999). Salmonella infection in a commercial line of developments. In Disease transmission through ducks; Experimental studies on virulence, intestinal international trade (MacDiarmid S, ed.). Revue colonization and immune protection. Epidemiology and Scientifique et Technique Office International des Épiyooties Infection 123, 121-132. 30, 149-164.

Beach JR and Davis DE (1927). Acute infection in Cobb SP, McVicar CM, Davies RH and chicks and chronic infection of the ovaries of hens Ainsworth H (2005). Fowl typhoid in caged layer caused by the fowl typhoid organism. Hilgardia 2, birds. Veterinary Record 157, 268. 411-424. Georgiev L, Zahariev T and Kaloyanov I (1978). Beaudette FR (1925). The possible transmission of The effect of low temperatures on the count and fowl typhoid through the egg. Journal of the American virulence of salmonellae in slaughtered birds Veterinary Medical Association 67, 741-745. Veterinarnomeditsinksi Nauki 15, 49-56.

Berchieri A Jnr, Murphy CK, Marston K and Ghafir Y, China B, Korsak N, Dierick K, Collard Barrow PA (2001). Observations on the persistence J-M , Godard C, de Zutter L and Daube G (2005). and vertical transmission of Salmonella enterica serovars Belgian surveillance plans to assess changes in Pullorum and Gallinarum in chickens: effect of Salmonella prevalence in meat at different production bacterial and host genetic background. Avian stages. Journal o f Food Protection 68, 2269-2277. Pathology 30, 221-231. Hoop RK and Albicker-Rippinger P (1997). Die Brant AW (1998). A brief history of the turkey. Salmonellagallinarum-pullorum-infektion des huhnes: World’s Poultry Science Journal 54, 365-373. Erfahrungen in der Schweiz (The infection with Salmonella gallinarum-pullorum in poultry: Experience Buchholz PS and Fairbrother A (1992). from Switzerland). Schweiyer Archiv fuer Tierheilkunde Pathogenicity of Salmonellapullorum in northern 139, 485-489. bobwhite quail and mallard ducks. Avian Diseases 36, 304-312. Johnson DC, David M and Goldsmith S (1992). Epizootiological investigation of an outbreak of Capita R, Álvarez-Astorga M, Alonso-Calleja C, pullorum disease in an integrated broiler operation. Moreno B and del Camino García-Fernández M Avian Diseases 36, 770-775. (2003). Occurrence of salmonellae in retail chicken carcasses and their products in Spain. International Komarov A (1932). Fowl typhoid in baby chicks. Journal o f Food Microbiology 81, 169-173. Veterinary Record 12, 1455-1457.

Christensen JP, Skov MN, Hinz KH and Maharjan M and Sharma AP (2000). Bisgaard M (1994). Salmonella enterica serovar Bacteriological quality of ground water in urban gallinarum biovar gallinarum in layers: Patan and antibiotic sensitivity against isolated enteric epidemiological investigations of a recent outbreak in bacteria. Journal o f the Nepal Medical Association 39, Denmark. Avian Pathology 23, 489-501. 269-274.

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union Maharjan M, Joshi V, Joshi DD and Poornima M Padungtod P and Kaneene JB (2006). Salmonella in (2006). Prevalence of Salmonella species in various food animals and humans in northern Thailand. raw meat samples of a local market in Kathmandu. International Journal of Food Microbiology 108, 346-354. Annals of the New York Academy of Sciences 1081, 249­ 256. Pennycott TW and Duncan G (1999). Salmonella pullorum in the common pheasant (Phasianus colchicus). Martinaglia G (1929). A note on Salmonella Veterinary Record 144, 283-287. gallinarum infection of ten-day old chicks and adult turkeys. Journal o f the South African Veterinary Medical Salem M, Odor EM and Pope C (1992). Pullorum Association 1, 35-36. disease in Delaware roasters. Avian Diseases 36, 1076­ 1080. Mayahi M, Sharma RN and Maktabi S (1995). An outbreak of blindness in chicks associated with Shivaprasad HL and Barrow PA (2008). Pullorum Salmonellapullorum infection. Indian Veterinary Journal disease and fowl typhoid. In Diseases of Poultry 12th 72, 922-925. Edition, Ed Saif YM, Blackwell Publishing. Pp. 620­ 636. McCullough NB and Eisele CW (1951). Experimental human salmonellosis. IV. Soomro AH, Khaskheli M, Bhutto MB, Shah G, Pathogenicity of strains of Salmonella pullorum Memon A and Dewani P (2010). Prevalence and obtained from spray-dried whole egg. Journal o f antimicrobial resistance of Salmonella serovars isolated Infectious Diseases 89, 259-265. from poultry meat in Hyderabad, Pakistan. Turkish Journal of Veterinary and Animal Sciences 34, 455-460. Mikoajczyk A and Radkowski M (2002). Salmonella spp. on chicken carcasses in processing Wigley P, Berchieri A, Page KL, Smith AL and plants in Poland. Journal o f Food Protection 65, 1475­ Barrow PA (2001). Salmonella enterica serovar 1479. Pullorum persists in splenic macrophages and in the reproductive tract during persistent, disease-free Mitchell RB, Garlock FC and Broh-Kahn RH carriage in chickens. Infection and Immunity 69, 7873­ (1946). An outbreak of gastroenteritis presumably 79. caused by Salmonella pullorum. Journal o f Infectious Diseases 79, 57-62. W illeberg P (2013). Chapter 5. Notification and animal disease surveillance. In: Risk assessments OIE (2013). World Animal Health Information regarding open trade in live animals to Iceland. Icelandic Database (WAHID) Interface. Available at: Food and Veterinary Authority (MAST), Reykjavik, http://www.oie.int/wahis 2/public/wahid.php/Wah Iceland. Pp. 59-90. idhome/Home, last accessed 1 July 2103.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 45. THE AGENT OF BOVINE SPONGIFORM ENCEPHALOPATHY

45.1. HAZARD IDENTIFICATION 45.1.1. Aetiological agent Since 1968, it has been prohibited to import meat and bone meal and greaves for use in feeding stuffs for livestock, and there has been a ban on feeding meat The disease agent causing bovine spongiform and bone meal to ruminants since 1978 and all food encephalopathy (BSE) is generally accepted to be a producing animals since 2001. In 2004, Iceland was prion, an abnormal and infectious protein that lacks recognized as a negligible BSE risk country by the genetic material. Prions are able to induce changes to OIE International Committee. Since 2000 samples the normal prion proteins in the infected animal to have been taken systematically every year. Until 2009 the abnormal infectious form (Bradley and Verwoerd samples were taken from cattle displaying behavioural 2004; Imran and Mahmood 2011). Accumulations of or clinical signs consistent with BSE and cattle more these abnormal prions cause spongiform changes in than 24 months of age within the categories of fallen the brain and neurological clinical signs. stock, casualty slaughter, and routine slaughter. Since 2010 the age criteria has been 30 months for fallen 45.1.2. Iceland status stock and casualty slaughter and 36 months for the category routine slaughter. Only in 1999, 2000, 2006, Bovine spongiform encephalopathy (BSE) has never 2009, and 2010 cattle were tested due to clinical signs, been reported in Iceland and is listed as a group A one each year (Willeberg 2013). notifiable disease in Act No 25/1993 (Willeberg 2013). Ongoing freedom is supported by general and 45.1.3. European Union status targeted surveillance (OIE 2013a). Table 42 (below) summarises the BSE status of the 28 countries of the European Union based on their official returns to the OIE.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 42: Status of bovine spongiform encephalopathy in European Union countries based on their official returns to the OIE (OIE 2013a)

EU M em ber Disease status O ther Austria Freedom Last reported September 2010 Belgium Freedom Last reported October 2006 Bulgaria Freedom Last reported March 2006 Croatia Freedom Has never occurred Cyprus Freedom Has never occurred Czech Republic Freedom Last reported May 2009 Denmark Freedom Last reported November 2009 Estonia Freedom Has never occurred Finland Freedom Last reported December 2001 France Present Disease restricted to certain zones Germany Freedom Last reported 2009 Greece Freedom Last reported 2001 Hungary Freedom Has never occurred Ireland Present Clinical disease Italy Freedom Last reported 2009 Latvia Freedom Has never occurred Lithuania Freedom Has never occurred Luxembourg Freedom Last reported November 2005 Malta Freedom Has never occurred Netherlands Freedom Last reported January 2011 Poland Present No clinical disease Portugal Present Clinical disease Romania Freedom Has never occurred Slovakia Freedom Last reported June 2010 Slovenia Freedom Last reported April 2007 Spain Present Disease restricted to certain zones Sweden Freedom Last reported February 2006 United Kingdom Present Clinical disease

45.1.4. Epidemiology BSE is a food-borne disease. In the United Kingdom, bans on feeding mammalian protein in ruminant feed and, subsequently, in all farmed BSE is a progressive nervous disease of cattle, livestock feed, resulted in a dramatic decrease in characterised by a long incubation period with the cases. This showed that the feed ban alone was minimum time from experimental oral infection to effective and no other epidemiologically significant detection of lesions in the brain being 32 months. route of infection exists (Wilesmith et al. 2010). However, the incubation period may be much longer than this, with a probable upper limit of about 8 years (Bradley and Verwoerd 2004). Recent experimental Infected animals are not contagious and it is accepted evidence shows that the incubation period and attack that horizontal transmission does not occur. rate are dependent on the infectious dose (Konold et Although vertical transmission cannot be ruled out al. 2012). Most natural cases of disease are seen in entirely, it can be regarded as insignificant since alone dairy cattle aged 4-5 years (Imran and Mahmood it could not perpetuate an outbreak (Bradley and 2011). A major epidemic of BSE began in the United Verwoerd 2004; Matthews and Adkin 2011; Simmons Kingdom in 1986 (Hillerton 1998). In total, 26 et al. 2012). Global eradication of BSE is therefore countries have reported confirmed cases of BSE likely to be achieved. since 1989 (OIE 2013b). Tissue infectivity data compiled and published by the The United Kingdom epidemic peaked in 1992 with a World Health Organization shows no detectable total of 37,490 cases (Hillerton 1998). Worldwide, the evidence of infectivity in bovine milk, blood, hides, total number of cases had reached 184,131 by skins, muscle or bone (WHO 2010). However, December 2004 but the number of annual cases reports of single cases of BSE in a livestock declined to 199 in 2005. During 2012, 3 cases were population have, historically, been met with severe reported in the United Kingdom and only 18 cases reactions by international markets and bans on beef for the rest of the world, down over 99 % from the and cattle imports. peak of cases reported in 1992 (OIE 2013b).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 45.1.5. Hazard identification conclusion During 2012, only 3 cases of BSE were reported in the UK and 18 cases in the rest of the world (OIE 2013a). Therefore, the likelihood of importing meat As noted above, Iceland has never reported a case of and meat products harbouring BSE prion is BSE and in 2004 was recognized as a negligible BSE extremely low risk country by the OIE International Committee (OIE 2013c). Although it is unlikely that imported meat and meat products may act as a vehicle for the The OIE also lists commodities that can be imported introduction of BSE, the extreme reaction likely to safely regardless of the BSE risk status of the meet the detection of a single case of this disease in exporting country. Safe commodities include Iceland dictates that the agent of BSE must be deboned skeletal muscle meat, dicalcium phosphate, identified as a potential hazard in imported meat and gelatine and collagen prepared from hides and skins, meat products derived from cattle. protein-free tallow, blood and blood by-products. Therefore, importing safe commodities as defined in the Code poses no animal or human health risk. 45.2. RISK ASSESSMENT 45.2.1. Entry assessment Reflecting the above, the likelihood of entry is assessed to be negligible. In countries affected by BSE, the introduction of feed controls for animals and removal of high risk tissues at slaughter has greatly reduced the prevalence 45.2.2. Risk estimation of BSE in cattle. The OIE recommends specified high risk materials such as the brain, spinal cord, eyes, Since the entry assessment is negligible, the risk is tonsils, distal ileum, skull, and vertebral column be estimated to be negligible and the agent of bovine removed at slaughter or processing and not be traded spongiform encephalopathy is not assessed to be a internationally. risk in unrestricted meat imports from the European Union.

References

Bradley R and Verwoerd DW (2004). Bovine OIE (2013a). World Animal Health Information spongiform encephalopathy. In: Coetzer JAW, Tustin Database (WAHID) Interface. Available at: RC (eds). Infectious Diseases o f Livestock. Oxford http://www.oie.int/wahis 2/public/wahid.php/Wah University Press, Oxford. Pp. 1408-1421. idhome/Home, last accessed 1 July 2103.

Hillerton JE (1998). Bovine spongiform OIE (2013b). Number of reported cases of bovine encephalopathy: Current status and possible impacts. spongiform encephalopathy (BSE) in farmed cattle Journal o f Dairy Science 81, 3042-3048. worldwide (except the UK). Available at: http://www.oie.int/animal-health-in-the-world/bse- Konold T, Arnold ME, Austin AR, Cawthraw S, specific-data/number-of-reported-cases-worldwide- Hawkins SAC, Stack MJ, Simmons MM, Sayers AR, excluding-the-united-kingdom/, last accessed 29 Dawson M, Wilesmith JW and Wells GAH (2012). August 2013. Bovine spongiform encephalopathy: the effect of oral exposure dose on attack rate and incubation period in OIE (2013c). Bovine spongiform encephalopathy cattle- an update. BioMed Central Research Notes. status of Member countries. Available at: Available at: http://www.biomedcentral.com/1756- http: / / www.oie.int/en/animal-health-in-the- 0500/5/674, last accessed 29 August 2013. world/official-disease-status/bse/list-of-bse-risk- status/, last accessed 29 August 2013. Matthews D and Adkin A (2011). Bovine spongiform encephalopathy: is it time to relax BSE- Simmons MM, Stack MJ, Konold T and Webster related measures in the context of international trade? K (2010). Chapter 2.4.6. Bovine spongiform Revue Scientifique et Technique Office International des encephalopathy. In: OIE Manual of Diagnostic Tests and Lpigooties 30, 107-117. Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: http: //www.oie.int/fileadmin/Home/eng/Health st Imran M and Mahmood S (2011). An overview of andards/tahm/2.04.06 BSE.pdf, last accessed 1 July animal prion diseases. Virology Journal, 8 (493). 2013. [Online] Available at: http: / / www.ncbi.nlm.nih.gov/pmc / articles /PMC322 8711/, last accessed 29 August 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union WHO (2010). WHO tables on tissue infectivity W illeberg P (2013). Chapter 5. Notification and distribution in transmissible spongiform animal disease surveillance. In: Risk assessments encephalopathies, World Health Organization. regarding open trade in live animals to Iceland. Icelandic Available at: Food and Veterinary Authority (MAST), Reykjavik, http: / / www.who.int/bloodproducts / tablestissueinfe Iceland. Pp. 59-90. ctivity.pdf, last accessed 29 August 2013.

Wilesmith JW, Ryan JBM , Arnold ME, Stevenson MA and Burke PJ (2010). Descriptive epidemiological features of cases of bovine spongiform encephalopathy born after July 31, 1996 in Great Britain. Veterinary Record 167, 279-286.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 46. ECHINOCOCCUS GRANULOSUS

46.1. HAZARD IDENTIFICATION 46.1.1. Aetiological agent 46.1.2. Iceland status

Echinococcus granulosus is a tapeworm (cestode) parasite. Echinococcosis/hydatidosis was last reported in At least 10 genotypes of Echinococcus granulosus are Iceland in 1979 and is listed as a group B notifiable recognised; type G1 is the common sheep genotype disease in Act No 25/1993 (Willeberg 2013). and most human infestations are caused by the G1 Ongoing freedom is supported by general genotype (Lavikainen et aL 2006). surveillance (OIE 2013).

46.1.3. European Union status

Table 43 (below) summarises the echinococcosis/hydatidosis status of the 28 countries of the European Union based on their official returns to the OIE.

Table 43: Status of echinococcosis/hydatidosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last reported June 2012 (wild) B ulgaria Present No clinical disease (domestic and wild) Croatia Freedom Last occurrence unknown Cyprus Present Clinical disease (domestic) Czech Republic Present No clinical disease (wild) Denmark Present Disease suspected (wild) Estonia Freedom Last occurrence unknown Finland Present No clinical disease (domestic and wild) France Present Disease restricted to certain zones (domestic and w ild) Germany Present Clinical disease (domestic and wild) Greece Present Disease restricted to certain zones (domestic) Hungary Present Disease restricted to certain zones (domestic) Ireland Freedom Has never occurred Italy Present Disease restricted to certain zones (wild) Latvia Freedom Last reported 2004 Lithuania Present No clinical disease (domestic and wild) Luxembourg Freedom Last occurrence unknown Malta Freedom Last occurrence unknown Netherlands Freedom Last reported 2008 Poland Present No clinical disease (domestic) Portugal Present No clinical disease (domestic) Romania Freedom Last reported 2004 Slovakia Present No clinical disease (wild) Slovenia Present Clinical disease (domestic) Spain Present Clinical disease Sweden Present Disease restricted to certain zones (wild) United Kingdom Present Clinical disease (domestic)

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 46.1.4. Epidemiology their viability at the extreme temperatures tested (- 10°C and 40°C). Dogs are the definitive host of Echinococcus granulosus. Eggs passed in dog faeces are eaten by the Imported meat and meat products are likely to be intermediate host (livestock species). Following subjected to at least several days storage at low hatching, larvae penetrate the gut wall and migrate to temperatures, which will affect scoleces survival. the liver or lungs where they develop into cysts with a Scoleces viability rapidly decreases at low and high diameter of up to 20 centimetres. Rarely, cysts may temperatures. Andersen and Loveless (1978) also develop in other organs and tissues. Scoleces reported that scoleces may survive up to 8 days at develop within cysts which may infect the definitive 1°C and 16 days at 10°C. Ohnishi et al. (1984) host if eaten. reported a shorter survival time of one day for scoleces stored in saline at 4°C. Hydatid cysts in the liver and lungs are tolerated without clinical signs. Surveillance for hydatids Because chilling is recognised to have a rapidly usually relies on post-mortem examination of the deleterious effect on the survivability of scoleces, the liver as cysts, if present, are readily detectable at this WHO/OIE recommends that material should be site. deep frozen at least to -20°C for at least 1-2 days to inactivate scoleces (Eckert et al. 2002). Humans may become accidental hosts of E. granulosus after ingesting tapeworm eggs that may (rarely) go on 46.1.5. Hazard identification conclusion to develop into hydatid cysts. E. granulosus can cause a severe (potentially fatal) disease in humans when Iceland is free from E. granulosus but it could be re­ the cyst stage develops in vital organs or a cyst introduced and establish through the importation of ruptures. Rupture of a cyst may cause fatal cysts within meat commodities that are subsequently anaphylaxis, or daughter cysts to develop in other fed to dogs. regions of the body (Taylor et al. 2007). Although E. granulosus is an important zoonotic disease, humans Meat and meat products would be derived from are considered dead-end hosts. animals that have passed ante-mortem and post­ mortem inspection in slaughter and processing plants Andersen and Loveless (1978) studied the effects of approved for export, which operate effective Good storage at constant temperatures on the survival of Manufacturing Practice (GMP) and Hazard Analysis scoleces from hydatid cysts of E. granulosus removed and Critical Control Point (HACCP) programmes. from infected sheep. They concluded that the Although post-mortem examination may significantly survival time of the scoleces at extreme temperatures reduce the likelihood of cysts being present in within samples of hydatid fluid was one hour at - imported meat and meat products, it may not detect 20°C, two hours at -10°C, one day at 40°C, and two recently infected animals. Therefore E. granulosus is hours at 50°C. The corresponding survival time for identified as a potential hazard in meat and meat intact cysts in liver and lungs was two hours at -20°C, products. eight hours at -10°C, four days at 40°C, and four hours at 50°C. 46.2. RISK ASSESSMENT These studies were supported by the later work of 46.2.1. Entry assessment Ohnishi et al. (1984) who reported that the longest survival time for scoleces in saline was two days at Since chilling, freezing, heating and mechanical 24°C, with all scoleces stored at 0°C destroyed within processes have a rapidly deleterious effect on the one day. Scoleces within their protective cysts survivability of scoleces, the likelihood of entry is survived much longer than the free scoleces in saline, assessed to be negligible for processed products. surviving for 6 days at 0°C, and 16 days at 12°C. Similarly, fresh chilled and frozen commodities that Both free scoleces and those within cysts rapidly lost contain muscle tissue only are assessed as having a their viability at 37°C and 0°C. negligible likelihood of harbouring viable scoleces. Furthermore, offal frozen to -20°C for at least 48 More recently Diker et al. (2008) examined scoleces hours is assessed to have a negligible likelihood of from liver hydatid cysts of naturally infected sheep introducing viable scoleces. and stored them in incubators at temperatures ranging from -10°C to 40°C. After two days at -10°C Viable unruptured cysts of E. granulosus are only likely the scoleces were fed to dogs and were unable to to survive in chilled offal. However, as noted in the cause infection. After 1 day at 40°C, scoleces were commodity definition (Section 4), offal is exclude unable to infect dogs. Scoleces stored at all other from the scope of this risk assessment. Therefore, temperatures remained viable and were able to infect the likelihood of entry for E. granulosus is assessed to dogs. Diker et al. concluded that scoleces rapidly lost be negligible.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 46.2.2. Risk estimation

Since the entry assessment is negligible, the risk is estimated to be negligible and E. granulosus is not assessed to be a risk in unrestricted meat imports from the European Union.

References

Andersen FL and Loveless RM (1978). Survival of Ohnishi K, Nakao M and Inaoka T (1984). protoscolices of Echinococcus granulosus at constant Viability and infectivity of protoscolices of temperatures. Journal of Parasitology 64, 78-82. Echinococcus multilocularis stored at different temperatures. International Journal of Parasitology 14, Diker AI, Tinar R and Senlik B (2008). Infectivity 577-580. of Echinococcus granulosus protoscolices under different conditions of temperature and humidity. Journal o f OIE (2013). World Animal Health Information Helminthology 82, 297-300. Database (WAHID) Interface. Available at: http://www.oie.int/wahis 2/public/wahid.php/Wah Eckert J, Gottstein B, Heath D and Liu F-J idhome/Home, last accessed 1 July 2103. (2002). Prevention of echinococcosis in humans and safety precautions. In: Eckert J, Gemmell MA, Meslin Taylor MA, Coop RL and Wall RL (2007). F-X, Pawlowski ZS (eds) WHO/OIE M anual on Echinococcus granulosus. In: Veterinary Parasitology. Echinococcosis in Humans and Animals: a Public Health Blackwell Publishing, Oxford. Pp. 376-377. Problem of Global Concern. WHO/OIE, Paris. Pp. 96­ 105. W illeberg P (2013). Chapter 5. Notification and animal disease surveillance. In: Risk assessments Lavikainen A, Lehtinen MJ, Laaksonen S, Agren regarding open trade in live animals to Iceland. Icelandic E, Oksanen A and Meri S (2006). Molecular Food and Veterinary Authority (MAST), Reykjavik, characterization of Echinococcus isolates of cervid Iceland. Pp. 59-90. origin from Finland and Sweden. Parasitology 133, 565­ 570.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 47. NEOSPORA CANINUM

47.1. HAZARD IDENTIFICATION 47.1.1. Aetiological agent 47.1.4. Epidemiology

Neospora caninum is a protozoan parasite, closely The complex life cycle of N. caninum involves three related to Toxoplasma gondii, that has emerged as a infectious stages. Tachyzoites and tissue cysts are the major cause of reproductive failure in cattle infectious stages found intracellularly in intermediate worldwide (Innes et al. 2005). hosts (Dubey et a l 2002). Tachyzoites are found primarily in the central nervous system whereas 47.1.2. Iceland status extraneural tissues (especially muscles) may contain tissue cysts (Peters et al. 2001; Dubey et al. 2004). The third infectious stage (the oocyst) is excreted in the Neospora caninum infection has never been reported in faeces of dogs and coyotes (McAllister et a l 1998; Iceland. Gondim et a l 2004a), and then sporulate outside the host (Lindsay et al 1999). It is believed that the 47.1.3. European Union status sporulated oocysts of N. caninum are as resistant to environmental conditions as the oocysts of the Evidence of N. caninum infection has been described closely related parasite T. gondii (Dubey 2004). This throughout the world. In the European Union complex life cycle is illustrated below in Figure 2. surveys have found evidence of N. caninum in Austria, Belgium, the Czech Republic, Denmark, France, Germany, Hungary, Ireland, Italy, the Netherlands, Poland, Portugal, Romania, Slovakia, Spain, Sweden, and the United Kingdom (Dubey et al. 2007).

Figure 2. Life cycle of Neospora caninum (from Dubey 1999)

Cattle are the most significant intermediate hosts of transplacentally transmitted parasites among all N. caninum, although there are reports of sheep, water known microbes in cattle. In certain herds, virtually buffalo, horses, and white-tailed deer also acting as an all calves are born infected (Dubey et a l 2007). intermediate host for this parasite (Dubey et a l 2007). Intermediate hosts become horizontally infected by Dogs (as well as coyotes and foxes) are the definitive ingesting sporulated N. caninum oocysts from the hosts for N. caninum (Dubey et a l 2007). Vertical environment (de Marez et a l 1999; Gondim et al transmission of Neosporosis was first recognized in 2004b; Trees et al. 2002). In addition vertical dogs (Bjerkås et al 1984; Dubey et al. 1990). (transplacental) transmission is common, with N. Transplacental transmission in experimentally caninum regarded as one of the most efficiently infected dogs has been demonstrated (Dubey and

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Lindsay 1989; Cole et aL 1995) although clinical signs responses, there is no evidence that N. caninum can of neonatal neosporosis are not seen until 5 to 7 infect humans (Dubey et al. 2007; McCann et al. weeks after birth (Dubey and Lindsay 1996), 2008). suggesting N. caninum is transmitted from the dam to the neonates toward the terminal stages of gestation 47.1.5. Hazard identification conclusion or postnatally via milk. However, vertical transmission of N. caninum in dogs is unlikely to persist in the absence of horizontal infection (Barber Infectious tissue cysts of N. caninum are found in the and Trees 1998). The majority of dogs become skeletal muscle of intermediate hosts (principally infected after birth, with higher prevalences cattle, but also small ruminants), and these have been documented in older than in younger dogs (Dubey et shown to transmit infection if fed to the definitive al. 2007). carnivorous host. N. caninum is identified as a potential hazard in unrestricted meat imports (beef, lamb, and goat meat) from the European Union. Horizontal transmission of N. caninum to dogs through consumption of tissues from infected intermediate hosts is well documented. In one 47.2. RISK ASSESSMENT report, 51% of 300 foxhounds fed bovine carcasses 47.2.1. Entry assessment were found to have N. caninum antibodies (Trees and Williams 2000). While consumption of aborted In an infected herd, widespread subclinical infection bovine foetuses does not appear to be an important with N. caninum would be expected. Tissue cysts (up source of N. caninum infection in dogs (Bergeron et al. to 107gm long) would not be visible at post-mortem 2001a, Dijkstra et al. 2002), the consumption of inspection. Although these infectious cysts are found bovine foetal membranes may be a source of N. primarily in the central nervous system (Dubey et al. caninum for dogs. The parasite has been found in 2007) there is evidence that they may also be found in naturally infected placentas (Shivaprasad et al. 1989; skeletal muscle. The likelihood of entry is assessed to Fioretti et al. 2000; Bergeron et al. 2001b), and dogs be very low. fed placentas from freshly calved seropositive cows may shed N. caninum oocysts (Dijkstra et al. 2001). Transmission of N. caninum infection from 47.2.2. Exposure assessment consumption of skeletal muscle from cattle (Gondim et al. 2002; Gondim et al. 2005; Cavalcante et al. 2011) Sarcocysts are inactivated following exposure to 55°C as well as from sheep and goats (Schares et al. 2001a; for 20 minutes (Fayer 1975), so cooked meat would Schares et al. 2001b) has been described. be unable to transmit infection to the definitive host.

Adult cows show no clinical signs of illness following For the life cycle of N. caninum to establish in Iceland, infection, and the majority have normal pregnancies. uncooked meat from infected cattle or small However, infected cattle are three times more likely ruminants would need to be fed to dogs in Iceland. to abort than uninfected cows. Calves of infected Although it is unlikely that imported raw meat would cows, although born clinically normal, have an 80 to be used specifically as dog food, scraps of meat 90 per cent chance of being N. caninum carriers. The generated in a domestic kitchen may be used in this female calves then have a high probability of way. infecting their own calves. As a result of this, it has been estimated that Neospora infection costs the There is a low likelihood of exposure. Australian dairy industry around $(Aus)85 million a year and the beef industry about $(Aus)25 million (Walker 2004). 47.2.3. Consequence assessment

Like cattle, the majority of dogs infected with Several epidemiological studies of dairy herds have Neospora show no clinical signs of disease. However, identified the presence of farm dogs as a risk factor in N. caninum infection in dogs can cause progressive the introduction of N. caninum (Mainar-Jaime et al. weakness and paralysis of one or both hind limbs, 1989; Paré et al. 1998; Schares et al. 2004; Corbellini et usually in pups under 6 months of age. The muscles al. 2006) and farm dogs defecating on feeding alleys of the affected leg waste away. In rare cases N. and on stored cattle food is reported on farms with caninum has also been reported to cause difficulty in neosporosis (Dijkstra et al. 2002). On these farms, swallowing, sudden death due to heart problems, dogs eating bovine placenta, uterine discharge, and pneumonia, and skin problems (Walker 2004). colostrum or milk has been suggested as an infection risk for dogs (Dijkstra et al. 2002). However, consumption of food scraps by farms dogs has not It was reported that two rhesus monkeys (Macaca been suggested by any authors as a risk factor for mulatto) had been successfully infected with N. introducing neosporosis in cattle. caninum (Barr et al. 1994), prompting concern that N. caninum may have zoonotic potential. However, although there is evidence of low level serological

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Since 2003, an average of around 160 dogs have been caninum, studies of the risk factors for introducing this imported into Iceland every year. Dogs infected with infection into a commercial herd suggest that there is N. caninum may shed oocysts erratically and a non­ a negligible likelihood of such exposure leading to the shedding seropositive bitch may transmit the establishment of this infectious disease in Iceland. infection vertically to her pups (Dubey et aL 2007). Although dogs imported into Iceland are subject to a The consequences of N. caninum introduction in the number of sanitary measures to manage their unrestricted import of meat are therefore assessed to associated biosecurity risks, it is unlikely that these be negligible. would have prevented the introduction of N. caninum. It is reasonable to suggest that the import of a live definitive host infected with N. caninum would be 47.2.4. Risk estimation much more likely to result in the establishment of infection in Iceland than the unrestricted import of Since the consequence assessment is negligible, the meat for human consumption. risk is estimated to be negligible and N. caninum is not assessed to be a risk in unrestricted meat imports Although feeding skeletal muscle from infected cattle, from the European Union. sheep, or goats has been shown experimentally to result in exposure of the definitive host (dogs) to N.

References

Barber JS and Trees AJ (1998). Naturally occurring Corbellini LG, Smith DR, Pescador CA, Schmitz vertical transmission of Neospora caninum in dogs. M, Correa A, Steffen DJ and Driemeier D (2006). International Journal o f Parasitology 28, 57-64. Herd-level risk factors for Neospora caninum seroprevalence in dairy farms in southern Brazil. Barr BC, Conrad PA, Sverlow KW, Tarantal AF Preventive Veterinary Medicine 74, 130-141. and Hendrickx AG (1994). Experimental fetal and transplacental Neospora infection in the nonhuman de Marez T, Liddell S, Dubey JP, Jenkins MC primate. Laboratory Investigation 71, 236-242. and Gasbarre L (1999). Oral infection of calves with Neospora caninum oocysts from dogs: humoral and Bergeron N, Fecteau G, Villeneuve A, Girard C cellular immune responses. International Journal of and Pare J (2001a). Failure of dogs to shed oocysts Parasitology 29, 1647-1657. after being fed bovine fetuses naturally infected by Neospora caninum. Veterinary Parasitology 97, 145-152. Dijkstra T, Eysker M, Schares G, Conraths FJ, Wouda W and Barkema HW (2001). Dogs shed Bergeron N, Girard C, Pare J, Fecteau G, Neospora caninum oocysts after ingestion of naturally Robinson J and Baillargeon P (2001b). Rare infected bovine placenta but not after ingestion of detection of Neospora caninum in placentas from colostrum spiked with Neospora caninum tachyzoites. seropositive dams giving birth to full-term calves. International Journal of Parasitology 31, 747-752. Journal o f Veterinary Diagnostic Investigation 13, 173-175. Dijkstra T, Barkema HW, Eysker M, Hesselink Bjerkås I, Mohn SF and Presthus J (1984). JW and Wouda W (2002). Natural transmission Unidentified cyst-forming sporozoon causing routes of Neospora caninum between farm dogs and encephalomyelitis and myositis in dogs. Zeitschrift Fur cattle. Veterinary Parasitology 105, 99-104. Parasitenkunde 70, 271-274. Dubey JP (1999). Neosporosis in cattle: biology and Cavalcante GT, Monteiro RM, Soares RM, Nishi economic impact. Journal of the American Veterinary SM, Alves Neto AF, Esmerini Pde O, Sercundes Medical Association 214, 1160-1163. MK, Martins J and Gennari SM (2011). Shedding of Neospora caninum oocysts by dogs fed different Dubey JP (2004). Toxoplasmosis—a waterborne tissues from naturally infected cattle. Veterinary zoonosis. Veterinary Parasitology 126, 57-72. Parasitology 179, 220-223. Dubey JP and Lindsay DS (1989). Transplacental Cole RA, Lindsay DS, Blagburn BL, Sorjonen Neospora caninum infection in dogs. American Journal of DC and Dubey JP (1995). Vertical transmission of Veterinary Research 50, 1578-1579. Neospora caninum in dogs. Journal of Parasitology 81, 208­ 211. Dubey JP and Lindsay DS (1996). A review of Neospora caninum and neosporosis. Veterinary Parasitology 67, 1-59.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Dubey JP, Koestner A and Piper RC (1990). Innes EA, Wright S, Bartley P, Maley S, Repeated transplacental transmission of Neospora Macaldowie C, Esteban-Redondo I and Buxton caninum in dogs. Journal of the American Veterinary D (2005). The host-parasite relationship in bovine Medical Association 197, 857-860. neosporosis. Veterinary Immunology andImmunopathology 108, 29-36 Dubey JP, Barr BC, Barta JR, Bjerkås I, Bjorkman C, Blagburn BL, Bowman DD, Lindsay DS, Dubey JP and Duncan RB (1999). Buxton D, Ellis JT, Gottstein B, Hemphill A, Confirmation that the dog is a definitive host for Hill DE, Howe DK, Jenkins MC, Kobayashi Y, Neospora caninum. Veterinary Parasitology 82, 327-333. Koudela B, Marsh AE, Mattsson JG, McAllister MM, Modry D, Omata Y, Sibley LD, Speer CA, Mainar-Jaime RC, Thurmond MC, Berzal- Trees AJ, Uggla A, Upton SJ, Williams DJL and Herranz B and Hietala SK (1999). Seroprevalence Lindsay DS (2002). Redescription of Neospora of Neospora caninum and abortion in dairy cows in caninum and its differentiation from related coccidia. northern Spain. Veterinary Record 145, 72-75. International Journal o f Parasitology 32, 929-946. McAllister MM, Dubey JP, Lindsay DS, Jolley Dubey JP, Sreekumar C, Knickman E, Miska WR, Wills RA and McGuire AM (1998). Dogs are KB, Vianna MCB, Kwok OCH, Hill DE, Jenkins definitive hosts of Neospora caninum. International MC, Lindsay DS and Greene CE (2004). Biologic, Journal of Parasitology 28, 1473-1478. morphologic, and molecular characterization of Neospora caninum isolates from littermate dogs. McCann CM, Vyse AJ, Salmon RL, Thomas D, International Journal o f Parasitology 34, 1157-1167. Williams DJL, McGarry JW, Pebody R and Trees AJ (2008). Lack of serologic evidence of Neospora Dubey JP, Schares G and Ortega-Mora LM caninum in Humans, England. Emerging Infectious (2007). Epidemiology and control of neosporosis and Diseases 14, 978-980. Neospora caninum. Clinical Microbiology Reviews 20, 323­ 367. Paré J, Fecteau G, Fortin M and Marsolais G (1998). Seroepidemiologic study of Neospora caninum Fayer R (1975). Effects of refrigeration, cooking, in dairy herds. Journal of the American Veterinary Medicine and freezing on Sarcocystis in beef from retail food Association 213, 1595-1598. stores. Proceedings of the Helminthological Society of Washington 42, 138-140. Peters M, Lutkefels E, Heckeroth AR and Schares G (2001). Immunohistochemical and Fioretti DP, Rosignoli L, Ricci G, Moretti A, ultrastructural evidence for Neospora caninum tissue Pasquali P and Polidori GS (2000). Neospora cysts in skeletal muscles of naturally infected dogs caninum infection in a clinically healthy calf: and cattle. International Journal o f Parasitology 31,1144­ parasitological study and serological follow-up. 1148. Journal of Veterinary Medicine B 47, 47-53. Schares G, Heydorn AO, Cuppers A, Conraths FJ Gondim LFP, Gao L and McAllister MM (2002). and Mehlhorn H (2001a). Cyclic transmission of Improved production of Neospora caninum oocysts, Neospora caninum: serological findings in dogs cyclical oral transmission between dogs and cattle, shedding oocysts. Parasitology Research 87, 873-877. and in vitro isolation from oocysts. Journal o f Parasitology 88, 1159-1163. Schares G, Heydorn AO, Cuppers A, Conraths FJ and Mehlhorn H (2001b). Hammondia heydorni-like Gondim LFP, McAllister MM, Pitt WC and oocysts shed by a naturally infected dog and Neospora Zemlicka DE (2004a). Coyotes (Canis latrans) are caninum NC-1 cannot be distinguished. Parasitology definitive hosts of Neospora caninum. International Research 87, 808-816. Journal o f Parasitology 34, 159-161. Schares G, Barwald A, Staubach C, Ziller M, Gondim LFP, McAllister MM, Anderson­ Kloss D, Wurm R, Rauser M, Labohm R, Drager Sprecher RC, Bjorkman C, Lock TF, Firkins LD, K, Fasen W, Hess RG and Conraths FJ (2003). Gao L and Fischer WR (2004b). Transplacental Regional distribution of bovine Neospora caninum transmission and abortion in cows administered infection in the German state of Rhineland-Palatinate Neospora caninum oocysts. Journal o f Parasitology 90, modeled by logistic regression. International Journal of 1394-1400. Parasitology 33, 1631-1640.

Gondim LFP, McAllister MM and Gao L (2005). Effects of host maturity and prior exposure history on the production of Neospora caninum oocysts by dogs. Veterinary Parasitology 134, 33-39.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Schares G, Barwald A, Staubach C, Ziller M, Trees AJ, McAllister MM, Guy CS, McGarry JW, Kloss D, Schroder R, Labohm R, Drager K, Smith RF and Williams DJL (2002). Neospora Fasen W, Hess RG and Conraths FJ (2004). caninum. oocyst challenge of pregnant cows. Potential risk factors for bovine Neospora caninum Veterinary Parasitology 109, 147-154. infection in Germany are not under the control of the farmers. Parasitology 129, 301-309. Walker B (2004). Neospora caninum infection in cattle. NSW Agriculture. Available at: Shivaprasad HL, Ely R and Dubey JP (1989). A http: / /www.dpi.nsw.gov.au/ data/assets /pdf file/ Neospora-like protozoon found in an aborted bovine 0020/160436/neospora.pdf, last accessed 28 placenta. Veterinary Parasitology 34, 145-148. September 2013.

Trees AJ and Williams DJL (2000). Neosporosis in the United Kingdom. International Journal of Parasitology 30, 891-893.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 48. TAENIA SPP. (T. OVIS, T. SAGINATA, AND T. SOLIUM)

48.1. HAZARD IDENTIFICATION 48.1.1. Aetiological agent Cysticerci are clear, translucent, pearly white or white. They are usually round to ovoid and approximately 1 cm or less in diameter, but can grow larger in areas Taeniasis refers to the adult stage of the parasite such as the subarachnoid space of the brain. Each living in the intestines of the definitive host. Humans fluid-filled vesicle contains a single invaginated are the definitive hosts for Taenia solium (the pork protoscolex, which usually appears as a single dense tapeworm) and T. saginata (the beef tapeworm), white body. Except in the eye, cerebral ventricles, whereas animals are the definitive hosts for T. ovis. and subarachnoid space of the brain, they are Taenia larvae are found in the muscles, central surrounded by a fibrous capsule. An organ may nervous system, and other tissues of the intermediate contain one to hundreds of cysticerci (Center for hosts. Larvae are more likely to cause disease than Disease Security and Public Health 2005). the adult tapeworms. Infection of with the larval form of T. solium, T. saginata, or T. ovis is referred to as cysticercosis (Center for Disease Security and Public 48.1.2. Iceland status Health 2005). Porcine cysticercosis has never been reported in Cysticercosis of farmed and wild animals is caused by Iceland and is listed as a group B notifiable disease in the larval stages (metacestodes) of cestodes Act No 25/1993 (Willeberg 2013). Ongoing freedom (tapeworms), the adult stages of which occur in the is supported by general surveillance (OIE 2013). intestine of humans and dogs or wild Canidae. Bovine cysticercosis (primarily in muscle) and porcine Neither ovine cysticercosis nor bovine cysticercosis cysticercosis (primarily in muscle, the central nervous are recognised in Iceland. system and the liver) are caused by the metacestodes (cysticerci) of the human cestodes Taenia saginata and T. solium, respectively. Cysticercosis and coenurosis 48.1.3. European Union status of sheep and goats (in the muscles, brain, liver and peritoneal cavity) are caused by T. ovis, T. multiceps and Taenia ovis is found throughout the world and bovine T. hydatigena, adults of which occur in the intestines of cysticercosis occurs virtually world-wide, but dogs and wild canids (Lloyd 2008). particularly in Africa, Latin America, Caucasian and South/Central Asian and eastern Mediterranean countries and the infection occurs in many countries in Europe (Center for Food Security and Public Health 2005; Lloyd 2008).

Table 44 (below) summarises the porcine cysticercosis status of the 28 countries of the European Union based on their official returns to the OIE.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Table 44: Status of porcine cysticercosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Not reported Belgium Freedom Last occurrence unknown Bulgaria Freedom Last reported 2009 Croatia Freedom Last reported 2004 Cyprus Freedom Last reported 1972 Czech Republic Freedom Last occurrence unknown Denmark Freedom Last occurrence unknown Estonia Freedom Last occurrence unknown Finland Freedom Last reported 1947 France Present No clinical disease Germany Freedom Last occurrence unknown Greece Freedom Last reported 1989 Hungary Freedom Last reported 2004 Ireland Not reported Italy Freedom Last reported 2010 (wild) Latvia Freedom Last reported 2004 Lithuania Freedom Last reported 2004 Luxembourg Freedom Last occurrence unknown Malta Freedom Last reported 2001 Netherlands Freedom Last occurrence unknown Poland Not reported Portugal Freedom Last reported 2002 Romania Freedom Last reported April 2011 (domestic); February 2011 (wild) Slovakia Freedom Last reported August 2007 Slovenia Freedom Last reported November 2007 Spain Present Clinical disease Sweden Freedom Has never occurred United Kingdom Freedom Last reported June 2008

48.1.4. Epidemiology eggs in contaminated food and water. Further, introducing eggs into the mouth via hands contaminated with faeces may cause infection (Taylor The domestic pig is the main intermediate host for T. et al. 2007b). solium, an important zoonosis in many pork-eating countries. Human neurocysticercosis occurs when larval parasitic cysts develop in the brain, a common Infected pigs usually show no clinical signs. In cause of epilepsy in developing countries. humans, tapeworms are generally insignificant, but Consumption of uninspected pig meat is the major may cause diarrhoea and abdominal discomfort. source of human taeniosis, and consequently, a major However, in the case of cysticerci of T. solium risk factor for human and pig cysticercosis (Allan et developing in humans, severe clinical signs may al. 2005). The transmission of T. solium eggs to pigs occur. These are dependent on the location and requires that pigs have access to human faeces and number of cysts in the organs, muscles or that people consume improperly cooked infected subcutaneous tissue. For instance, cysts in the brain intermediate host (pork) (Taylor et al. 2007b). cause mental disturbances, epilepsy and may be fatal (Taylor et al. 2007b). The larval stage of T. solium (Cysticercus cellulosae) occurs in the skeletal and cardiac muscles, central Cattle act as the intermediate hosts for T. saginata, the nervous system, and liver of pigs. Humans are the so-called beef tapeworm of humans who are the definitive host, but also may act as an intermediate definitive host. An infected human may pass millions host whereby cysticerci occur in muscles, of eggs daily in faeces, which may survive several subcutaneous tissues and central nervous system. months on pasture. After eggs are ingested by cattle, Cysticercosis, whether pig or human, occurs larval tapeworms develop as cysts in any striated following ingestion of eggs in human faeces. Person- muscle (Taylor et al. 2007a; Lloyd 2008). In cattle, to-person transmission occurs by the ingestion of most T. saginata cysticerci are found in the masseter muscles, tongue, heart and diaphragm (Center for

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Disease Security and Public Health 2005). Occasional 48.1.5. Hazard identification conclusion reports indicate that buffaloes and deer may sometimes act as intermediate hosts (Nuttall 1991). Taenia solium can be transmitted to humans that eat contaminated pig meat and pig meat products, T. saginata does not spread between bovines. Humans especially if imported from countries where the acquire infection from ingestion of raw or disease prevalence is high. T. solium is identified as a undercooked meat containing live cysticerci (Taylor et potential hazard in imported pig meat and pig meat aL 2007a). Only infected humans can spread eggs. products.

The animal infected with the larval stage of T. saginata Taenia saginata causes a zoonotic disease that occurs in ('Cysticercus bovis) generally shows no clinical signs. many countries. Infection can be transmitted to Further, the public health significance of infection humans who eat contaminated commodities, in with the tapeworm is limited since clinical symptoms particular, those imported from countries where the are benign (Taylor et aL 2007a). However, in addition prevalence is high. Accordingly, T.saginata is to minor public health issues, cysticercosis may cause identified as a potential hazard in meat and products significant economic losses to the cattle industry containing meat derived from cattle, buffaloes, and because cysts act as space occupying lesions, become deer. caseous or calcify and thus reduce the economic value of the carcass, and possibly carcase Taenia ovis can be transmitted to canines from condemnation at slaughter. There are limitations to undercooked sheep meat. T. ovis is identified as a the detection of infected carcasses, particularly those potential hazard in imported sheep meat and sheep with light infections with meat inspection being more meat products. efficient at detecting heavily infected carcasses rather than light infections (Allan et al. 2005; Taylor et al. 2007a). 48.2. RISK ASSESSMENT 48.2.1. Entry assessment T. saginata is present in the human population essentially worldwide. Very few countries are free of Tapeworms of T. solium are frequently introduced T. saginata although the prevalence is low in countries inside infected people. However, the organisms have in Australasia, Europe and North America because not been reported in pigs in Iceland. These standards of sanitation are high, and meat is inspected organisms are uncommon in most developed and generally cooked before consumption. countries. However, imported meat and products containing meat derived from pigs may harbour Sheep and goats are the intermediate hosts of Taenia viable cysticerci. This is despite post-mortem ovis, with dogs, wild carnivores and, rarely, cats inspection of the carcass which is inevitably a recognised as the definitive hosts (Center for Disease compromise between detection of cysticerci and the Security and Public Health 2005). preservation of the economic value of the carcass. Introduction through imported pig meat is likely to occur despite post-mortem inspection. Therefore, the Taenia ovis occurs worldwide, mainly in rural areas of countries with large sheep populations. The larval likelihood of entry for T. solium assessed to be non- stage of T. ovis (Cysticercus ovis) is found mainly in the negligible. muscles of sheep and goats. Meat from an infected sheep or goat may have multiple cysts, mainly in the Similarly, Taenia saginata is likely to be constantly heart, the diaphragm, and the jaws. T. ovis eggs being introduced into Iceland in infected people. passed in canine faeces can remain infective for up to However, due to a high standard of sanitation, the 12 months. Once ingested by sheep or goats the organism appears to not be completing its life cycle young larvae hatch out of the eggs in the gut, go endemically. This organism is found worldwide and through the intestinal wall, reach the blood stream imported meat and products containing meat derived and migrate to a muscle, where they encyst. The from cattle, buffaloes and deer may harbour viable cysts need 10 to 12 weeks to complete development. cysticerci, despite post-mortem inspection. The cysts may remain infective for dogs for up to one Introduction of T. saginata through imported meat is year. Dogs and other canids become infected when likely to occur despite post-mortem inspection. eating insufficiently cooked meat contaminated with Therefore, the likelihood of entry is assessed to be cysts. non-negligible.

Cysticercus ovis is not pathogenic for sheep or goats and Taenia ovis may be found in the meat of subclinically usually the infection causes no clinical disease. infected sheep and goats. The likelihood of entry of However, infections have a substantial economic T. ovis is therefore also non-negligible. impact resulting from carcase condemnation at slaughter. Infection of dogs with T. ovis is also usually benign (Junquera 2013).

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union 48.2.2. Exposure assessment T. ovis eggs in dog faeces. T. ovis could subsequently develop in intermediate hosts (sheep and goats) providing an ongoing source of infection to dogs. Imported pig meat containing viable larvae of T. solium is unable to transmit infection to pigs. Pigs can only be infected from exposure to eggs in human faeces. 48.2.3. Consequence assessment For this reason, exposing pigs to contaminated pig meat poses no risk of infection. Consequently, the As indicated above, establishment of T. ovis in Iceland likelihood of exposure is assessed to be negligible. would have no clinical consequences for either the definitive host or the intermediate host. However, Similarly, imported meat containing viable T. saginata infections in sheep and goats may have a substantial would not transmit infection to animals. Only humans economic impact resulting from carcase who eat uncooked contaminated meat, become condemnation at slaughter. The consequences are infected and shed eggs in their faeces could expose therefore assessed to be non-negligible. animals. Because standards of sanitation are high, humans infected from eating raw meat are unlikely to 48.2.4. Risk estimation pose any greater risk of exposing animals to the parasite than international travelers. The likelihood of exposure for T. saginata is assessed to be negligible. Since entry, exposure, and consequence assessments are non-negligible, the risk is estimated to be non- negligible and T. ovis is assessed to be a risk in Humans and livestock would not become infected unrestricted sheep (and goat) meat imports from the with T. ovis through eating contaminated sheep or European Union. goat meat. However, if a dog were to eat uncooked or undercooked contaminated meat then a patent infection could establish resulting in the shedding of

References

Allan JC, Avila G, Brandt J, Correa D, Del Brutto Nuttall W (1991). Bovine cysticercosis in New OH, Dorny P, Flisser A, Garcia HH, Geerts S, Zealand. Surveillance 18 (1), 20-21. Ito A, Kyvsgaard NC, Maravilla P, McManus DP, Meinardi H, Murrell KD, Nash TE, OIE (2013). World Animal Health Information Pawïowski ZS and Rajshekhar V (2005). Database (WAHID) Interface. Available at: WHO/FAO/OIE Guidelines for the Surveillance, http://www.oie.int/wahis 2/public/wahid.php/Wah Prevention and Control of Taeniosis/Cysticercosis. idhome/Home, last accessed 1 July 2103. OIE, Paris. Available at: http: / /www.oie.int/doc /ged /d11245.pdf, last Taylor MA, Coop RL and Wall RL (2007a). accessed 30 August 2013. Parasites of the locomotory system, Taenia saginata. In: Veterinary Parasitology, Blackwell publishing, Center for Food Security and Public Health Oxford. Pp. 121-123. (2005). Taenia infections. Available at: http: / / www.cfsph.iastate.edu /Factsheets / pdfs/ taeni Taylor MA, Coop RL and Wall RL (2007b). a.pdf last accessed 27 September 2013. Parasites of the locomotory system, Taenia solium. In: Veterinary Parasitology, Blackwell publishing, Oxford. Junquera P (2013). Cysticercus ovis, sheep measles, Pp. 343-345. parasitic tapeworm of sheep and goats. Biology, prevention and control. Available at: W illeberg P (2013). Chapter 5. Notification and http://parasitipedia.net/index.php?option=com con animal disease surveillance. In: Risk assessments tent&view=article&id=2579&Itemid=2861, last regarding open trade in live animals to Iceland. Icelandic accessed 27 September 2013. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90. Lloyd S (2008). Chapter 2.9.5. Cysticercosis. In: OIE Manual o f Diagnostic Tests and Vaccines fo r Terrestrial Animals. OIE, Paris. Available at: http://www.oie.int/fileadmin/Home/eng/Health st andards /tahm/2.09.05 CYSTICERCOSIS.pdf, last accessed 22 September 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 49. TRICHINELLA SPP.

49.1. HAZARD IDENTIFICATION 49.1.1. Aetiological agent 49.1.2. Iceland status

Trichinellosis in humans is caused by eating raw or Trichinellosis has never been reported in Iceland and undercooked meat from Trichinella-infected is listed as a group B notifiable disease in Act No domestic animals or game. Trichinella are nematodes 25/1993 (Willeberg 2013). Ongoing freedom is in the family Trichinellidae. Twelve genotypes of supported by general and targeted surveillance (OIE Trichinella are recognised, and eight have been 2013). designated species status including Trichinella spiralis, T. native, T. britovi, T. pseudospiralis, T. murrelli, T. nelson, T. papuae, and T. yimbabwensis (Taylor et al. 2007; 49.1.3. European Union status Gajadhar and Forbes 2012). Table 45 (below) summarises the trichinellosis status of the 28 countries of the European Union based on their official returns to the OIE.

Table 45: Status of trichinellosis in European Union countries based on their official returns to the OIE (OIE 2013)

EU M em ber Disease status O ther Austria Freedom Last occurrence unknown Belgium Present In one or more zones (wild) B ulgaria Present No clinical disease (domestic and wild) Croatia Present No clinical disease (domestic and wild) Cyprus Freedom Has never occurred Czech Republic Freedom Last reported 1961 (domestic); June 2011 (wild) Denmark Freedom Last reported 1930 E stonia Present Clinical disease (wild) F inland Present No clinical disease (domestic and wild) France Present Disease restricted to certain zones (domestic and w ild) Germany Present No clinical disease (domestic or wild) Greece Freedom Last reported 2009 Hungary Present No clinical disease (wild) Ireland Present No clinical disease (wild) Italy Present Disease restricted to certain zones (domestic and w ild) Latvia Present No clinical disease (wild) L ithuania Present No clinical disease (domestic and wild) Luxembourg Freedom Last occurrence unknown Malta Freedom Has never occurred Netherlands Present Clinical disease (wild) Poland Present No clinical disease (domestic and wild) Portugal Freedom Last occurrence unknown R om ania Present Disease restricted to certain zones (domestic and w ild) Slovakia Present No clinical disease (wild) Slovenia Present Clinical disease (wild) Spain Present In one or more zones (domestic and wild) Sweden Present Clinical disease (wild) United Kingdom Freedom Last reported 1975

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 49.1.4. Epidemiology Horsemeat has increasingly been implicated in the transmission of trichinellosis to humans (Bessonov et al. 2011). However, it is not known how horses The adult nematodes live in the small intestine of a become infected although this may be as a result of wide range of flesh-eating animals, including humans. eating contaminated feeds, either from rodent Larvae released from mature females migrate into the carcasses within manufactured feeds, or faecal systemic circulation and invade muscle tissue. The contamination from animals with patent infections. larvae of most Trichinella species then become encapsulated in host musculature where they remain infective for years (Gajadhar and Forbes 2012). An important factor in the control of trichinellosis is Development resumes when muscle containing the ensuring that swill or waste human food intended for encysted trichinae is eaten by another host. The feeding to pigs has been heat treated to inactivate trichinae are liberated in the stomach and intestine trichinae. Further on-farm controls include secure and moults, maturing in about one week (Taylor et aL buildings/feed storage, rodent control, quick disposal 2007). of dead animals and quarantine with serological testing before introducing new animals (International Commission on Trichinellosis 2011). T. spiralis is distributed worldwide in temperate regions and commonly associated with domestic pigs. T. nativa occurs in polar bears, walrus, and other 49.1.5. Hazard identification conclusion mammalian carnivores of arctic and sub-arctic regions. T. nelsoni occurs in tropical Africa and has Transmission of T. spiralis in pig meat is widely been isolated from mammalian carnivores and documented. Trichinellosis is recognised in a sporadically from wild pigs. T. britovi is found in wild number of countries in the European Union. carnivores and occasionally in pigs or horses Trichinella spp. is therefore identified as a potential throughout temperate regions of Europe, Asia and hazard in imported pig meat and pig meat products. Africa. T. murrelli is found in mammalian carnivores of North America (Gajadhar and Forbes 2012). In 49.2. RISK ASSESSMENT contrast to these species, T. pseudospiralis, T. papuae, and T. gimbabwensis do not become encapsulated in 49.2.1. Entry assessment host musculature. T. pseudospiralis has a worldwide distribution with mammals and raptorial birds as Ante-mortem and post-mortem inspection is unlikely principal hosts. T.papuae and T. gimbabwensis are to detect infections in pigs presented for slaughter found in crocodiles in Papua New Guinea and because clinical signs of infection are generally not Zimbabwe respectively (Taylor et aL 2007; Gajadhar noticeable. At meat inspection, heavy larval and Forbes 2012). infections may occasionally be seen with the naked eye as tiny greyish white spots in those muscles that Clinical signs of infection in naturally infected larvae favour. For example, the main predilection animals are rarely seen (Gajadhar et aL 2006). sites where large numbers of larvae accumulate are However, if hundreds of larvae are eaten, the the diaphragmatic, intercostals, and masseter muscles, intestinal infection is often associated with enteritis and the tongue (Gamble 1997; Taylor et al. 2007). and diarrhoea. This is followed by a massive larval Trichinae remain infectious for months in meat. invasion of muscle 1-2 weeks later causing acute myositis, fever, and myocarditis. Unless humans are The likelihood of entry of trichinae is assessed to be treated with an anthelmintic and anti-inflammatory non-negligible. drugs, heavy infestations may frequently be fatal as a result of paralysis of respiratory muscles (Taylor et aL 49.2.2. Exposure assessment 2007).

Humans who eat contaminated pig meat products Humans become infected from eating raw or that are undercooked or raw are at risk of exposure to undercooked pork or pork products. Wildlife viable trichinae. Likewise, carnivorous and commonly become infected from predation or omnivorous mammals such as pigs, cats, dogs, and cannibalism. Feeding on carrion also may transmit rodents that feed on contaminated products may also infection since encapsulated trichinae survive months become infected. This may be through intentional in decomposing flesh. Rats in piggeries maintain a exposure as part of a pet’s diet, from scavenging secondary cycle, which may on occasion pass to pigs scraps in the case of wild mammals, or from backyard or vice versa from eating infected flesh or faeces pigs being fed waste food. Infected pet cats and dogs (Taylor et al. 2007). are likely to be dead-end hosts whereas rodents may disseminate infection. Should pigs be fed raw Meat is the usual vehicle for spreading T. spiralis. Pigs contaminated imported product, they would become are usually infested by the practice of feeding them infectious to other pigs, rodents and humans. garbage containing meat scraps, although they may contract the parasite from eating rodent carcasses or faeces (of rodents or pigs) (MacDiarmid 1991).

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union The likelihood of exposure is assessed to be non- This notwithstanding, heavily contaminated pig meat negligible. poses a significant public health threat. Humans eating imported contaminated pig meat could cause 49.2.3. Consequence assessment sporadic infections. Further, discarded raw scraps could lead to an increased spread and prevalence in wildlife reservoirs that could lead to more frequent Consuming contaminated meat could lead to human spillover events into domestic pigs. These infected infection, with some cases of severe illness, even pigs entering the food chain may lead to sporadic death, if not treated. However, in most cases there human infections. would be no discernible illness. Epidemiological studies have shown that the majority of infections in Establishment would be likely to have a negligible domestic pigs are well below one larva per gram of effect on the pig industry, as infected animals rarely tissue. This amount of infection is generally show clinical signs. Infections in other mammals are considered not to pose a public health risk. Post­ also likely to go unnoticed. Despite negligible mortem surveys suggest that there are large numbers consequences for animals, the consequences of of humans with subclinical or undiagnosed infections. introduction and establishment are assessed to be It is highly likely that low level pig infections not non-negligible for public health reasons. detected even when inspection programmes are in place are responsible for many of these human infections (Gamble 1997). Indeed, because of test 49.2.4. Risk estimation sensitivity limitations, slaughter inspection methods are designed to prevent clinical trichinellosis in Since entry, exposure, and consequence assessments humans and are not designed to prevent infection are non-negligible, the risk is estimated to be non- entirely (International Commission on Trichinellosis negligible and Trichinella spp. is assessed to be a risk in 2011). unrestricted pig meat imports from the European Union.

References

Bessonov AS, Cuperlovic K, Gajadhar AA, MacDiarmid SC (1991). The importation into New Gamble AA, van Knapen F, Noeckler K, Zealand of meat and meat products. A review of the Schenone H, Zhu X (2011). Recommendations on risks to animal health. Ministry of Agriculture and methods for control of Trichinella in domestic and Fisheries New Zealand, Wellington, New Zealand. wild animals intended for human consumption. Available at: International Commission on Trichinellosis. Pp. 20. http: / / www.biosecurity.govt.nz / files / regs / imports / r isk/meat-meat-products-ra.pdf, last accessed 2 Gajadhar A and Forbes L (2012). Chapter 2.1.16. September 2013. Trichinellosis. In: OIE Manual of Diagnostic Tests and Vaccines fo r Terrestrial Animals, OIE, Paris. Available at: OIE (2013). World Animal Health Information http://www.oie.int/fileadmin/Home/eng/Health st Database (WAHID) Interface. Available at: andards/tahm/2.01.16 TRICHINELLOSIS.pdf, last http://www.oie.int/wahis 2/public/wahid.php/Wah accessed 4 July 2013. idhome/Home, last accessed 1 July 2103.

Gajadhar AA, Scandrett WB and Forbes LB Taylor MA, Coop RL and Wall RL (2007). (2006). Overview of food- and water-borne zoonotic Trichinella spiralis. In: Veterinary Parasitology. Blackwell parasites at the farm level. Revue Scientifique et Technique Publishing, Oxford. Pp. 324-326. Office International des Épizooties 25, 595-606. W illeberg P (2013). Chapter 5. Notification and Gamble HR (1997). Parasites associated with pork animal disease surveillance. In: Risk assessments and pork products. Revue Scientifique et Technique Office regarding open trade in live animals to Iceland. Icelandic International des Épizooties 16, 496-506. Food and Veterinary Authority (MAST), Reykjavik, Iceland. Pp. 59-90. International Comission on Trichinellosis (2011). Control and prevention in pork and other meat from food animals. Available at: http://www.trichinellosis.org/Control and Prevent! on.html, last accessed 30 August 2013.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 50. APPENDIX 1 - ICELANDIC REGULATION NO. 448/2012 No. 448/2012 23 May 2012 REGULATION on measures to prevent the introduction of animal diseases and infected products to Iceland

"CHAPTER III General provisions on imports Article 4 Import permits The Ministry ofFisheries and Agriculture may, upon the recommendation of MAST, permit the import of goods listed in Art. 3, cf. Art. 10 of Act No. 25/1993, on Animal Diseases and their Prevention, as subsequently amended, provided it is deemed proven that they will not carry any infectious agents which cause diseases in animals or humans and the conditions set for the importation are satisfied, cf. however, Art. 7. When applying in the first instance to import a raw or unsterilised product as referred to in the first paragraph, an importer must provide the Ministry of Fisheries and Agriculture with the necessary information on the product for consideration and approval before the product is dispatched from the country of export. An importer of raw products must always apply for a permit to the Minster of Fisheries and Agriculture and provide, for the consideration of MAST, an import declaration, information on the country of origin and production, the type of product and producer, and the required certificates, as provided for in Art. 5. All import of animal products from states outside the European Economic Area must go through border check points. Article 5 Raw foods and dairy products Imported foods which are listed under classifications 0202, 0203, 0204, 0207, 0208, 0210, 1601 and 1602, cf. Appendix I, to the Customs Act, No. 88/2005, which the Minister has authorised for import to Iceland as referred to in Art. 4 and which have not received satisfactory heat treatment must be accompanied by the following certificates: a. an official certificate of origin and health, in the case of products from

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union producers outside the European Economic Area; b. an official certificate confirming that the animals from which the products derive were not given growth-enhancing substances during rearing, in the case of products from producers outside the European Economic Area; c. a certificate confirming that the products have been stored at a temperature no higher than -18°C for a month prior to customs clearance; d. an official certificate confirming that the animals from which the products derive were slaughtered in slaughterhouses and the products processed in processing plants authorised in the European Economic Area, in the case of products from producers outside the European Economic Area; e. an official certificate confirming that the products are free of salmonella bacteria; f. meat products and by-products and dairy products and eggs must satisfy the provisions of the current Regulation on food contaminants; g. the product labelling must comply with current rules on labelling, advertising and promotion of foodstuffs. Imported foods in classifications 0210 and 1601, which have been treated with one of the following methods, must be accompanied by an official certificate of origin and health, if the products come from producers outside of the European Economic Area, together with confirmation that the product has been treated as follows: a. with heat treatment where the product is in air-tight packaging with an Fc value of 3.00 or more, or so that the core temperature reached 72°C for 15 seconds, or b. natural fermenting and maturing. The meat must have received treatment involving fermenting or maturing, and have an aw value which does not exceed 0.93 and pH value which does not exceed 6.0. Raw ham must have been curedfor at least 190 days and raw loins at least 140 days, or c. meat dried, processed for storage. The meat must have received treatment which, in the estimation of MAST, is comparable to those treatments in subparagraphs a and b above. Imported cheeses in customs classifications 0406.2000 and 0406.3000 must have received appropriate treatment so that the cheese matter has been heat treated at least to 48°C, the product must have been storedfor at least 6 months at a temperature of not less than 10°C and a humidity of less than 36%. The product must be accompanied by an official certificate of origin and health, in the case of products from producers outside of the European Economic Area, and confirmation that the product has received appropriate treatment. Article 6 Petfood Import of petfoods which are manufactured in compliance with the

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union requirements which apply to such production in the European Economic Area is authorised if the food has been treated as follows and confirmation thereof is provided in the producer's statement upon registering the product, if it comes from a producer in the European Economic Area, cf. Art. 5 of Act No. 22/1994, on Control of Feed, Fertiliser and Seed, or in the case of a third state, in a certificate recognised by the EU which is produced upon import: a. chewing bones made of hide or leather must have been heated sufficiently to kill infectious organisms (including salmonella); b. canned food must have been heated to a minimum Fc value of 3.0 in airtight packaging; c. dairy products must be pasteurised; d. other petfoods than the above-mentioned must have been heated to a minimum core temperature of 90°C. The importer must inform MAST of the proposed importation with at least 48 hours notice, cf. Appendix 7 of Reg. No. 340/2001, on Control of Feed, as subsequently amended. Article 7 Import of used agricultural machinery An importer of used agricultural machinery and equipment, including horse trailers and other equipment which has been used in agriculture, cf. subparagraph j of Art. 3, must always apply for an import permit from the Minister of Fisheries and Agriculture; such a permit must be obtained before the products in question are dispatched from the country of export. The Minister of Fisheries and Agriculture may authorise the import of machinery as referred to in the first paragraph upon the recommendation of MAST, provided it is deemed to be proven that it does not carry infectious agents which could cause animal diseases. An application for an import permit shall be accompanied, for consideration by MAST, by information on the country of origin and manufacture, the type, the manufacturer, and an official veterinary certificate that adequate cleaning and disinfection has been carried out in the country of export. If the requirements of the first and second paragraph are not satisfied, MAST shall not recommend the import of machinery listed in the first paragraph. MAST may, however, recommend the import of machinery on the condition that special disinfection be carried out at the importer's cost and under the supervision of MAST, if it is possible to clean and disinfect machinery at the port of entry. Article 8 Importer's responsibility The importer of a product must ensure that all necessary certificates accompany the product upon importation and shall bear all costs which may be

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union incurred in obtaining certificates andfrom the disinfection measures which must be satisfied for importation, including the sampling and testing considered necessary by MAST. Article 9 International risk assessment The recommendations of MAST concerning disease control must be based on risk assessment which, among other things, takes account of lists of the World Organisation for Animal Health (OIE) of A and B diseases and other international standards and guidelines. The implementation of this Article shall be consistent with the provisions of the Agreement on the Application of Sanitary and Phytosanitary Measures in Annex 1A of the Agreement Establishing the World Trade Organization.”

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 51. APPENDIX 2 - CHAPTER 2.1 OF THE OIE TERRESTRIAL ANIMAL HEALTH CODE

Chapter 2.1.

IMPORT RISK ANALYSIS

Article 2.1.1.

Introduction

The importation of animals and animal products involves a degree of disease risk to the importing country. This risk may be represented by one or several diseases or infections.

The principal aim of import risk analysis is to provide importing countries with an objective and defensible method of assessing the disease risks associated with the importation of animals, animal products, animal genetic material, feedstuffs, biological products and pathological material. The analysis should be transparent. This is necessary so that the exporting country is provided with clear reasons for the imposition of import conditions or refusal to import.

Transparency is also essential because data are often uncertain or incomplete and, without full documentation, the distinction between facts and the analyst's value judgements may blur.

This chapter alludes to the role of the OIE with respect to the Agreement on the Application of Sanitary and Phytosanitary Measures (the so-called SPS Agreement) of the World Trade Organization (WTO), provides definitions and describes the OIE informal procedure for dispute mediation.

This chapter provides recommendations and principles for conducting transparent, objective and defensible risk analyses for international trade. The components of risk analysis described in that chapter are hazard identification, risk assessment, risk management and risk communication (Figure 1).

Fig. 1 .The four components of risk analysis

The risk assessment is the component of the analysis which estimates the risks associated with a hazard. Risk assessments may be qualitative or quantitative. For many diseases, particularly for

Import Risk Assessment. Ruminant, swine, and poultry meat and meat products from the European Union those diseases listed in this Terrestrial Code where there are well developed internationally agreed standards, there is broad agreement concerning the likely risks. In such cases it is more likely that a qualitative assessment is all that is required. Qualitative assessment does not require mathematical modelling skills to carry out and so is often the type of assessment used for routine decision making. No single method of import risk assessment has proven applicable in all situations, and different methods may be appropriate in different circumstances.

The process of import risk analysis usually needs to take into consideration the results of an evaluation of Veterinary Services, zoning, compartmentalisation and surveillance systems in place for monitoring of animal health in the exporting country. These are described in separate chapters in the Terrestrial Code.

Article 2.1.2.

Hazard identification

The hazard identification involves identifying the pathogenic agents which could potentially produce adverse consequences associated with the importation of a commodity.

The potential hazards identified would be those appropriate to the species being imported, or from which the commodity is derived, and which may be present in the exporting country. It is then necessary to identify whether each potential hazard is already present in the importing country, and whether it is a notifiable disease or is subject to control or eradication in that country and to ensure that import measures are not more trade restrictive than those applied within the country.

Hazard identification is a categorisation step, identifying biological agents dichotomously as potential hazards or not. The risk assessment may be concluded if hazard identification fails to identify potential hazards associated with the importation.

The evaluation of the Veterinary Services, surveillance and control programmes and zoning and compartmentalisation systems are important inputs for assessing the likelihood of hazards being present in the animal population of the exporting country.

An importing country may decide to permit the importation using the appropriate sanitary standards recommended in the Terrestrial Code, thus eliminating the need for a risk assessment.

Article 2.1.3.

Principles of risk assessment

1. Risk assessment should be flexible to deal with the complexity of real life situations. No single method is applicable in all cases. Risk assessment should be able to accommodate the variety of animal commodities, the multiple hazards that may be identified with an

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union importation and the specificity of each disease, detection and surveillance systems, exposure scenarios and types and amounts of data and information. 2. Both qualitative risk assessment and quantitative risk assessment methods are valid. 3. The risk assessment should be based on the best available information that is in accord with current scientific thinking. The assessment should be well-documented and supported with references to the scientific literature and other sources, including expert opinion. 4. Consistency in risk assessment methods should be encouraged and transparency is essential in order to ensure fairness and rationality, consistency in decision making and ease of understanding by all the interested parties. 5. Risk assessments should document the uncertainties, the assumptions made, and the effect of these on the final risk estimate. 6. Risk increases with increasing volume of commodity imported. 7. The risk assessment should be amenable to updating when additional information becomes available.

Article 2.1.4.

Risk assessment steps

1. Entry assessment

Entry assessment consists of describing the biological pathway(s) necessary for an importation activity to introduce pathogenic agents into a particular environment, and estimating the probability of that complete process occurring, either qualitatively (in words) or quantitatively (as a numerical estimate). The entry assessment describes the probability of the ‘entry’ of each of the potential hazards (the pathogenic agents) under each specified set of conditions with respect to amounts and timing, and how these might change as a result of various actions, events or measures. Examples of the kind of inputs that may be required in the entry assessment are:

a. Biological factors ■ species, age and breed of animals ■ agent predilection sites ■ vaccination, testing, treatment and quarantine. b. Country factors ■ incidence or prevalence ■ evaluation of Veterinary Services, surveillance and control programmes and zoning and compartmentalisation systems of the exporting country. c. Commodity factors ■ quantity of commodity to be imported ■ ease of contamination ■ effect of processing ■ effect of storage and transport.

If the entry assessment demonstrates no significant risk, the risk assessment does not need to continue.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union 2. Exposure assessment

Exposure assessment consists of describing the biological pathway(s) necessary for exposure of animals and humans in the importing country to the hazards (in this case the pathogenic agents) from a given risk source, and estimating the probability of the exposure(s) occurring, either qualitatively (in words) or quantitatively (as a numerical estimate).

The probability of exposure to the identified hazards is estimated for specified exposure conditions with respect to amounts, timing, frequency, duration of exposure, routes of exposure, such as ingestion, inhalation or insect bite, and the number, species and other characteristics of the animal and human populations exposed. Examples of the kind of inputs that may be required in the exposure assessment are:

a. Biological factors ■ properties of the agent. b. Country factors ■ presence of potential vectors ■ human and animal demographics ■ customs and cultural practices ■ geographical and environmental characteristics. c. Commodity factors ■ quantity of commodity to be imported ■ intended use of the imported animals or products ■ disposal practices.

If the exposure assessment demonstrates no significant risk, the risk assessment may conclude at this step.

3. Consequence assessment

Consequence assessment consists of describing the relationship between specified exposures to a biological agent and the consequences of those exposures. A causal process should exist by which exposures produce adverse health or environmental consequences, which may in turn lead to socio-economic consequences. The consequence assessment describes the potential consequences of a given exposure and estimates the probability of them occurring. This estimate may be either qualitative (in words) or quantitative (a numerical estimate). Examples of consequences include:

a. Direct consequences ■ animal infection, disease and production losses ■ public health consequences. b. Indirect consequences ■ surveillance and control costs ■ compensation costs ■ potential trade losses ■ adverse consequences to the environment.

4. Risk estimation

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union Risk estimation consists of integrating the results from the entry assessment, exposure assessment, and consequence assessment to produce overall measures of risks associated with the hazards identified at the outset. Thus risk estimation takes into account the whole of the risk pathway from hazard identified to unwanted outcome.

For a quantitative assessment, the final outputs may include:

o estimated numbers of herds, flocks, animals or people likely to experience health impacts of various degrees of severity over time; o probability distributions, confidence intervals, and other means for expressing the uncertainties in these estimates; o portrayal of the variance of all model inputs; o a sensitivity analysis to rank the inputs as to their contribution to the variance of the risk estimation output; o analysis of the dependence and correlation between model inputs.

Article 2.1.5.

Principles of risk management

1. Risk management is the process of deciding upon and implementing measures to achieve the Member Country's appropriate level of protection, whilst at the same time ensuring that negative effects on trade are minimized. The objective is to manage risk appropriately to ensure that a balance is achieved between a country's desire to minimize the likelihood or frequency of disease incursions and their consequences and its desire to import commodities and fulfil its obligations under international trade agreements. 2. The international standards of the OIE are the preferred choice of sanitary measures for risk management. The application of these sanitary measures should be in accordance with the intentions in the standards.

Article 2.1.6.

Risk management components

1. Risk evaluation - the process of comparing the risk estimated in the risk assessment with the Member Country's appropriate level of protection. 2. Option evaluation - the process of identifying, evaluating the efficacy and feasibility of, and selecting measures to reduce the risk associated with an importation in order to bring it into line with the Member Countries appropriate level of protection. The efficacy is the degree to which an option reduces the likelihood or magnitude of adverse health and economic consequences. Evaluating the efficacy of the options selected is an iterative process that involves their incorporation into the risk assessment and then comparing the resulting level of risk with that considered acceptable. The evaluation for feasibility normally focuses on technical, operational and economic factors affecting the

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union implementation of the risk management options. 3. Implementation - the process of following through with the risk management decision and ensuring that the risk management measures are in place. 4. Monitoring and review - the ongoing process by which the risk management measures are continuously audited to ensure that they are achieving the results intended.

Article 2.1.7.

Principles of risk communication

1. Risk communication is the process by which information and opinions regarding hazards and risks are gathered from potentially affected and interested parties during a risk analysis, and by which the results of the risk assessment and proposed risk management measures are communicated to the decision-makers and interested parties in the importing and exporting countries. It is a multidimensional and iterative process and should ideally begin at the start of the risk analysis process and continue throughout. 2. A risk communication strategy should be put in place at the start of each risk analysis. 3. The communication of the risk should be an open, interactive, iterative and transparent exchange of information that may continue after the decision on importation. 4. The principal participants in risk communication include the authorities in the exporting country and other stakeholders such as domestic and foreign industry groups, domestic livestock producers and consumer groups. 5. The assumptions and uncertainty in the model, model inputs and the risk estimates of the risk assessment should be communicated. 6. Peer review is a component of risk communication in order to obtain scientific critique and to ensure that the data, information, methods and assumptions are the best available.

Import Risk Assessment: Ruminant, swine, and poultry meat and meat products from the European Union