Infectología al Día

Knowledge about bacterial and viral pathogens present in wild mammals in Chile: a systematic review

Sebastián Llanos-Soto1 and Daniel González-Acuña2

1Laboratorio de Enfermedades Knowledge about viral and bacterial pathogens present in wild mammals in Chile: y Parásitos de Fauna Silvestre. Departamento de Ciencia Animal. a systematic review Facultad de Ciencias Veterinarias, Universidad de Concepción, Chile. This study organizes all available information about viral and bacterial pathogens of wild mammals in Chile. This 2Laboratorio de Vida Silvestre. Departamento de Ciencia Animal. was done in order to identify pathogens that have been well-documented and recognize those that have not been Facultad de Ciencias Veterinarias, properly studied, determine the number of articles that have been published annually about this topic and identify Universidad de Concepción, Chile. regions in Chile that concentrate the highest and lowest number of studies concerning viral and bacterial pathogens. A total of 67 scientific articles published in peer-reviewed journals from 1951 to 2018 were selected for revision. Conflicts of interest. None declared. Results indicate that the number of publications has increased per decade but there are years in which no articles were published. Most studies addressed Leptospira, rabies, hantavirus, Mycobacterium avium paratuberculosis Submitted: June 10, 2018 (MAP) and distemper. Rodentia, Carnivora, Chiroptera and Cetartiodactyla were the most studied mammal orders. Accepted: October 25, 2018

Information about presence/absence of pathogens was found for 44 wild mammal species. Research was mainly A Spanish version of this review carried out in central and southern Chile and the most commonly employed methods for pathogen diagnosis were was published in Rev Chilena serology and molecular techniques. Overall, research in wild mammals has been directed towards the evaluation Infectol, 2019; 36 February (1). of zoonotic diseases, while vector-borne and non-zoonotic diseases have been mostly neglected by the scientific Corresponding author: community over the years. Daniel González Acuña Keywords: Bacteria; Chile; mammals; virus; zoonoses. Facultad de Ciencias Veterinarias Palabras clave: Bacteria; Chile; mamíferos; virus; zoonosis. Universidad de Concepción Av. Vicente Méndez 595 Chillán, Chile. Phone: +56 422208739 Fax: +56 422208739 [email protected] Introduction they will probably continue to do so in the future7. These factors may lead to habitat fragmentation, ecosystem dis- nowledge about the presence of infectious ruption and over-exploitation of species, which added to diseases in wildlife is pivotal to understand the the expansion of human and domestic animal populations potential consequences that they might have on in areas close to natural habitats, might contribute to the K 1 transmission of infectious diseases from free-living wild species conservation and their threat to human health . Anthropogenic factors, such as the introduction of alien animals to domestic animals and humans8-11. species, climate change, habitat loss and fragmentation The objectives of this review were to (1) gather and and human encroachment in natural areas might increase organize all the information available in articles published the risk of disease transmission from wild reservoirs to in peer-reviewed journals involving the assessment of domestic animals and humans2,3. viral and bacterial infections in Chilean wild mammals, Diseases that are transmitted between animals and (2) identify which pathogens have been prioritized by the humans are called zoonoses and cause both economical local scientific community and which have received little and social losses, especially in underdeveloped and devel- to no attention, (3) evaluate the number of articles pub- oping countries3. Zoonotic pathogens, such as rabies and lished annually about the prevalence of viral and bacterial hantavirus, have their origin in mammal reservoirs and are pathogens in wild mammal hosts and (4) recognize the considered extremely important for public health systems number of studies developed in this topic in the different because of their consequences on human health4,5. In this regions of Chile. context, affected individuals may have their health com- promised by zoonotic diseases, and in many cases, they might be wrongly characterized as common infections Materials and Methods or even go unnoticed to health care institutions6. Urban- ization and industrial activities, such as agriculture and Peer-reviewed scientific publications evaluating the forestry, have intensified in Chile during recent years and prevalence of viral and bacterial pathogens in Chilean wild

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mammals were searched and listed following the Preferred (1), Microbiotheria (1), Chiroptera (11), Xenarthra (3), Reporting Items for Systematic Reviews and Meta-Analy- Rodentia (63), Cetartiodactyla (47), Lagomorpha (2) and ses (PRISMA) declaration guidelines12. Articles published Carnivora (20). Three species were excluded from the in Spanish or English from January 1950 through July review because their distribution was restricted to Ant- 2018 were selected for revision. Data from unpublished arctica (Ommatophoca rossii) or their presence in Chile literature (grey literature) was excluded from this study has yet to be confirmed (Stenella attenuate and Stenella (i.e., abstracts, books, local bulletins and presentations at longirostris). Research studies that included previously scientific conferences) based on the fact that these types diagnosed cases of viral and bacterial infections in their of scientific documents do not often undergo a rigorous analysis (e.g., positive cases of rabies diagnosed by the peer-review process prior to publication. This means that Chilean National Institute of Public Health, ISP in Span- the accuracy, reliability and quality of the findings being ish) were also included in this review. Pathogens were presented in these documents cannot be ensured. Viral and listed from highest to lowest in the discussion depending bacterial agents were considered pathogenic when there on the number of articles available in the literature related was information available in the literature indicating their to that specific pathogen. ability to cause disease in animals, humans or both. The revision considered pathogens present in free-living native and introduced mammalian species, with the exception of Results domestic animals and individuals maintained in captivity in zoos, farms and exhibition centers. Publications about A total of 67 publications about viral and bacterial pathogens found in mammals from the Chilean Antarctic pathogens in Chilean mammals were included in this Territory were also excluded from the review, as they review. From the literature assessed, 34 studies evalu- have been already reviewed in another scientific article13. ated the prevalence of viral pathogens and 35 studies Google Scholar (https://scholar.google.cl/), Scielo concerned bacteria. Information about presence/absence Scientific Library (http://www.scielo.cl/) and PubMed of pathogens was found for 44 species from the Rodentia (https://www.ncbi.nlm.nih.gov/pubmed/) databases were (15), Carnivora (10), Chiroptera (9), Cetartiodactyla (8), used to conduct an extensive search for publications. Didelphimorphia (1) and Lagomorpha (1) orders (Figure Keywords “bacteria”, “bacterial”, “Brucella”, “corona- 1). Details about the results of this review are indicated virus”, “Corynebacterium”, “distemper”, “hantavirus”, in the Supplementary Table 1. “herpesvirus”, “infectious disease”, “Leptospira”, “My- Overall, the number of studies addressing the infec- cobacterium”, “Mycoplasma”, “parvovirus”, “pathogen”, tion or exposure to viral or bacterial pathogens in wild “picornavirus”, “rabies”, “retrovirus”, “Salmonella”, mammals has increased per decade (Figure 2), however, “vector-borne”, “viral”, “virus”, “zoonosis” AND during the last decade there are years in which the number “Carnivora”, “Cetartiodactyla”, “Chiroptera”, “Didelphi- of articles published ranges from 0 to 2 (i.e., 2010, 2012 morphia”, “Lagomorpha”, “mammal”, “Microbiotheria”, and 2016). Publications dedicated to each pathogen varied “Paucituberculata”, “Rodentia”, “wildlife”, “Xenarthra” in number, most studies were related to Leptospira (16 AND “Chile” were inputed in independent searches. studies), rabies virus (12 studies), hantavirus (10 studies), These same keywords were also employed to perform Mycobacterium avium paratuberculosis (8 studies) and searches in Spanish to account for publications in local canine distemper virus (6 studies). journals. Articles that were not available for download The first study to record the presence of pathogens in online were physically searched in the libraries from wild mammals in Chile was performed by Neghme et al. in Universidad de Chile, Universidad Austral, Pontificia 1951 and involved the evaluation of Leptospira in brown Universidad Católica de Chile and Universidad de Con- rats (Rattus norvegicus) captured in a slaughterhouse cepción. Information about prevalence for each pathogen from the Metropolitana region14. Rodentia was the most was organized and listed in a supplementary table using studied mammal order with 27 publications assessing the Microsoft® Excel 2010. The table included data about presence of viral and bacterial pathogens. A high number mammal host, pathogen characterization (e.g., serotype, of articles were dedicated to investigate the long-tailed genetic lineage, class), region in Chile where the study pygmy rice rat (Oligoryzomys longicaudatus), with 19 was developed and technique used for diagnosis. Data scientific publications involving the evaluation of Lep- from selected publications was analyzed using line graphs tospira and hantavirus in this species. Order Carnivora to evaluate a potential trend in the number of articles (16), Chiroptera (12) and Cetartiodactyla (12) have also published per decade since 1951 and identify the most received attention from the scientific community. Only studied mammal orders in Chile. two studies involved a lagomorph species and a single Data was searched for a total of 150 mammal species article concerned a member of the Didelphimorphia order. from eight orders: Didelphimorphia (2), Paucituberculata No study determined infection with viral or bacterial

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Figure 1. Number of scien- tific studies regarding viral or bacterial infections in different mammal orders from 1980 to 2018.

Figure 2. Number of scienti- fic studies assessing the pre- valence of viral or bacterial infections in wild mammals in Chile from 1951 to 2018.

pathogens in members of the orders Paucituberculata, in the Tarapacá and the Atacama regions. Research has Microbiotheria and Xenarthra. not been carried out in the Arica y Parinacota region. A A high number of studies of viral and bacterial total of 7 and 4 studies have been developed in the regions infections were focused in southern and central Chile, of Aysén and Magallanes, respectively. particularly from the Coquimbo to the Los Lagos regions. Most studies applied serological methods for pathogen The most studied regions were the Los Ríos region with diagnosis in mammal hosts, such is the case of the dis- 24 studies, the Metropolitana region with 14 studies and temper virus and parvovirus and the bacterium Brucella, the Los Lagos region with 13 studies. Only three studies which have been only assessed using serology. These in rabies and a single one in hantavirus were carried out methods were also commonly applied in research studies in the Maule Region. Research studies including mammal involving hantavirus in wild rodents. The application of species from the northern regions of Chile are lacking, molecular methods to detect pathogens in wild mammals with two studies in the Antofagasta region and a sigle one has raised in the last two decades in Chile, which has

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been reflected in an increase in the use of these type of Reports indicating the presence of Leptospira in techniques for diagnosing viruses and bacteria in wild other mammal orders are scarce in comparison to the mammals. The use of other methods, such as direct information available for rodents. This bacterium has immunofluresence, bacterial culture and histopathology been documented in only two carnivore species; the South has been mostly restricted for the specific diagnosis of American sea lion (Otaria flavescens) and the American certain pathogens. mink (Neovison vison)9,28. The interaction between wild animals and domestic reservoirs (i.e., dogs and livestock) can act as an important mechanism for the ocurrence of Discussion leptospirosis cases in human inhabited environments29. Future studies dedicated to evaluate the role of wild spe- Wild mammals have played a crucial role as reservoirs cies in the maintainance and transmission of Leptospira of infectious diseases in developing countries and have will make an important contribution to the understanding been involved in the occurrence of spill-over epizootic about the dynamics of this pathogens in natural and urban events in human populations3. These events negatively areas of the country. impact public health systems in these countries and result in important economic losses3,4. In Chile, most scientists Rabies virus and governamental institutions have destined their efforts Rabies is a cosmopolitan zoonotic disease of great in studying those zoonotic agents considered as a serious importance for public health worldwide30. All mammals threat to human health, such as Leptospira, rabies virus are susceptible to rabies virus but only chiropterans and and hantavirus. Pathogens restricted to animal hosts and carnivores are capable of successfully maintain and trans- which do not represent a threat to humans (e.g., canine mit the infection in the long-term30. In Chile, confirmed distemper virus) have only recently began to receive cases of rabies are characterized by the ISP in different scientific attention and, in consequence, information antigenic variants using specific monoclonal antibodies. available about them is much more limited. Each variant represents an assemblage of viruses within a serotype that possesses defined antigenic properties31. This Leptospira method of antigenic characterization of rabies has been Leptospirosis is a cosmopolitan zoonotic disease widely applied in the country to study the geographical of great relevance for human health, particularly in and temporal distribution of the virus32,33. developing and low-income countries, where sanitary The first case of human rabies in Chile was reported conditions and resources destined for disease diagnosis in 1879 and surveillance in domestic and wild species and prevention are limited15. The agent responsible for has been performed since 1929 by the ISP (at the time causing this disease is Leptospira, a bacterial pathogen called “Instituto Bacteriológico de Chile”)34,35. The efforts capable of infecting a variety of mammal hosts and sur- of the ISP allowed to identify wildlife and domestic vive for several months in the environment in areas with species prevalent to the virus, amongst them livestock, warm and humid climate conditions16. lagomorphs, rodents, carnivores and chiropterans33,34. Rodents play an important role in the maintenance and However, active surveillance of rabies began following dissemination of pathogenic and non-pathogenic Lepto- the first oubreak of this disease in bats, more specifically, spira to other mammal species in urban and rural areas in the brazilian free-tailed bat (Tadarida brasiliensis) in of Chile, including humans and domestic animals17,18. To 198533. After this event, rabies cases have been mainly this date, evidence of infection by this pathogen have been reported in bats33,36. shown in nine rodent species present in the country; the To this date, five antigenic variants have been identified degu (Octodon degus), olive-colored akodont (Abrothrix in Chile, including the canine antigenic variant AgV2 olivaceus), long-haired akodont (Abrothrix longipilis), and four variants associated with insectivorous bats; the Darwin’s leaf-eared mouse (Phyllothis darwini), long- antigenic variant AgV4 Tadarida, antigenic variant AgV6 tailed pygmy rice rat (O. longicaudatus), black rat Lasiurus, antigenic variant AgV3 Myotis chiloensis and an (Rattus rattus), brown rat (R. norvergicus), house mouse antigenic variant AgV not typed for Histiotus33,37,38. The (Mus musculus) and long-clawed mole mouse (Geoxus most common variant registered in Chile from 2008 to valdivianus)17-27. Rattus norvegicus and R. rattus are 2013 has been AgV439. Antigenic variants are described to particularly relevant reservoirs due to the high prevalence be host-specific38,40 , but recent studies suggest that there of Leptospira documented in these species in rural areas could be cross-species spillover transmission of rabies of the country18,27. This bacterium has been described in variants in bats32,38,41,42. wild mammals in south-central areas of Chile, and more Six of the eleven species of bats distributed in the specifically in the Metropolitana, Los Ríos, Los Lagos country have been described to be infected with the virus; and Aysén regions. the big-eared brown bat (Histiotus macrotus), small big-

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eared brown bat (Histiotus montanus), mouse-eared bat Oligoryzomys longicaudatus is the most important (M. chiloensis), eastern red bat (Lasiurus borealis), hoary reservoir of the Andes virus in Chile, being responsible bat (Lasiurus cinereus) and Brazilian free-tailed bat (T. of disseminating the hantavirus to humans along its brasiliensis)32,33,37,43. Considering the available scientific distributional ranged from the Copiapó to the Magallanes information, T. brasiliensis and L. cinereus remain the regions54,57-59. Oligoryzomys longicaudatus has been cha- most relevant reservoirs of bat rabies in Chile32,36,37,41,43,44. racterized as a high mobility species, which increases the Escobar et al. (2013) indicate that both T. brasiliensis risk of encountering humans throughout its wide home and L. cinereus, and their respective antigenic variants of range (320-4800m2)60. This species can be found in close rabies (AgV4 and AgV6), share similar ecological niches proximity to urban areas, inhabiting humid environments in Chile and their distribution is limited by the presence of and areas covered by bushes near water sources60. Increase natural ecological barriers, such as the Andes Mountains in wild rodent population density in peri-urban areas has to the east and the Pacific Ocean to the west32. Bat rabies been linked to an elevation in the number of cases of han- seems to follow a seasonal pattern with peaks of positivity tavirus cardiopulmonary syndrome (HCPS) in humans51. during hot season (October-March) and decrease in colder It has been suggested that the explosive increase in the months33,39. This could be related to a reduction in bat number of rodents during years of synchronized flowering activity during winter in the Southern hemisphere and of native bamboo, particularly Chusquea quila, might be therefore less chance of rabies transmission among bats implicated in the occurrence of hantavirus outbreaks in and from bats to other susceptible species33,39,45. humans due to an increased available of food provided The increase in population size and density of dogs, by these plants51,52. Most cases of hantavirus infection in added to the presence of bat (mainly T. brasiliensis) in Chile occur near towns in rural and peri-urban areas where urban areas, have raised the risk of rabies transmission O. longicaudatus is present and people are constantly events from bats to dogs across the country46,47. This is exposed to become infected with the virus55,61,62. particularly important for central Chile, which possesses a high number of bat-related antigenic variants and an Mycobacterium increased richness of chiropteran species33. Highly popu- Mycobacterium avium subp. paratuberculosis (MAP) lated human settlements, such as the large cities located in is an important pathogen of cattle and small ruminants, the Metropolitana, Maule, Biobío and Valparaíso regions, responsible for causing important economic losses in posses an elevated risk of rabies transmission between animal production worldwide63. In Chile, native ungulates animals and humans and concentrate the higher number are at continuous risk of becoming infected with MAP of human cases33,39,47. Rabies cases have been reported due to the high prevalence of this pathogen reported in in wild carnivores in Chile in years prior to 199048, livestock, particularly in southern areas of the country64. however, insectivorous bats are currently considered the The guanaco (Lama guanicoe), the Southern pudu (Pudu most important reservoir of rabies in the country with puda), the Chilean Huemul (Hippocamelus bisulcus) and the 97.31% (1339/1376) of positive cases reported by the European hare (Lepus europaeus) have been reported the ISP from 1985 to 201232. The importance of bats as to carry this bacterium in Chile65-69. MAP-infected guana- rabies reservoirs and the increasing population of stray cos did not display any health-related issues and European dogs in in urban areas rise concern about the current risk hares did not present microscopic or macroscopic lesions of rabies transmission from bats to dogs and, ultimately, associated with the infection65,68. In the case of the huemul, humans beens47. the bacterium presented similar molecular characteristics to MAP isolates commonly reported in livestock in Chile, Hantavirus suggesting that the latter are spreading the infection to Seven rodent species have been found to be exposed or huemul populations70. The situation is concerning for this infected with the Andes virus in Chile; the olive-colored endangered deer species, particularly in central Chile, akodont (A. olivaceus), long-haired akodont (A. longipi- where the population of huemuls is facing severe con- lis), Darwin’s pericote (P. darwini), Southern big-eared servation issues and its habitat is being disturbed by the mouse (Loxodontomys micropus), black rat (R. rattus), presence of domestic animals71. Similarly, MAP infections brown rat (R. norvergicus) and long-tailed pygmy rice were documented in three Southern pudus found in areas rat (O. longicaudatus)49-57. Reports of hantavirus belong commonly occupied by dairy cattle67. Currently, there to areas in south and central Chile, particularly from is no information about pathological findings of MAP the Coquimbo to Magallanes regions. To this date, the infection in free-ranging pudúes, however, this bacterium presence of hantavirus in the country has been restricted was indicated as the cause of death for an individual solely to rodents and has not been possible to identify the maintained in captive settings66. virus in wild species from other orders, such as the case Infections with MAP have also been reported in intro- of marsupials and chiropterans54. duced deer species in southern Chile, such as the red deer

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(Cervus elaphus) and fallow deer (Dama dama), which Chilean wildlife is lacking. Mora et al. (2015) found that could be transmitting the pathogen to livestock and vice guignas in Chiloé were infected with feline leukemia versa72,73. The European wild boar (Sus scrofa) is currently (FeLV) and feline immunodeficiency viruses (FIV) distributed in rural and protected areas of south-central with no apparent clinical signs85. Nucleotide sequences Chile and is considered as a carrier of MAP in Europe74,75. obtained from FeLV and FIV in guignas were almost Currently, there have not been reports of MAP infection identical to those found in domestic cats, suggesting that in this species in the country. The role that introduced cats may be playing an important role in the transmission ungulates species are playing in the transmission of MAP of retroviruses to wild felids. Some feline species, such as and other pathogens to native wildlife and livestock is a the guigna, inhabit in areas close to human settlements and topic that still needs to be explored in Chile. they ocassionally predate on poultry86, which increases the risk of interacting with infected domestic cats. Retroviru- Canine distemper virus ses have been detected in the cougar and other large felids Distemper is a viral disease prevalent in dogs all over in North America87, however, the presence of these viral the world and capable causing severe illness in wild car- agents in populations of cougars and most of the native nivores76. A wide range of species from different families, wild felids species in Chile still needs to be addressed. such as the Canidae, Felidae, Hyaenidae, Mustelidae, Information about viral and bacterial pathogens in Ursidae, Vivirridae and Procyonidae have been reported native ruminants is very scarce. Bovine viral diarrhea to be exposed or infected to canine distemper virus (CDV), virus (BVDV) was detected in the southern pudu and two in some cases, with major population declines76,77. CDV Chilean huemuls were found to be exposed to the virus88,89. currently possesses an endemic status in urban and rural Similar to MAP, BVDV isolates from the southern pudu populations of dogs in Chile, with seroprevalences that share molecular characteristics with viruses circulating range from 51 to 73%10,78. Dogs have been indicated in cattle, suggesting that livestock are acting as dissemi- as the source of CDV outbreaks in populations of the nators of pathogens to native wildlife in Chile70,88. Other South American gray fox (Lycalopex griseus) in central pathogens present in livestock, such as bovine rhinotra- Chile10,79,81 and may be a threat to populations of the cheitis virus (BoHV-1) and Brucella spp., were assessed endangered Darwin’s fox (Lycalopex fulvipes) in south- in the Chilean huemul using serological methods, but no central Chile82. individual were found to be exposed89. To this date, there are no study that applied methods to There is no information about infections with viral directly detect distemper virus in Chilean wildlife, howe- or bacterial pathogens in aquatic carnivores, such as ver, serological surveys have found exposure to the virus members of the Otariidae, Phocidae and Mustelidae in the American mink (N. vison), South American sea lion families, except for the South American sea lion (O. (O. flavescens), South American gray fox (L. griseus) and flavescens) and the invasive American mink (N. vison). Andean fox (Lycalopex culpaeus)8,9,79,80,81. There is no Furthermore, cetaceans have been mostly overlooked information about infection or exposure to CDV in wild by the local scientific community, with only one viral felids and indigenous mustelids in the country. disease being identified in Chile90,91. The Chilean dolphin Neglected pathogens and wild mammal species (Cephalorhynchus eutropia), black porpoise (Phocoena This section includes pathogens that have received spinipinnis), bottle-nosed dolphin (Tursiops truncatus) little attention from the scientific community in Chile were found to present marks on their bodies typical of and information about their presence in natural hosts is tattoo skin disease, an affection that might lead to neo- currently lacking or inexistent. natal mortality and have negative consequences on host Parvoviruses have been detected in a wide range of population dynamics90,91. No other pathogens have been wild carnivores around the world, belonging to the Ca- reported in cetaceans distributed in Chile, despite the fact nidae, Felidae and Mustelidae families83. In Chile, canine that exposure to cetacean morbillivirus and Brucella sp. (CPV) and feline parvoviruses (FPV) are recognized was described in species living along the Peruvian section affections of dogs and cats, respectively84. Serological of the Pacific Ocean92-94. assessments of CPV in L. culpaeus, L. griseus and O. flavescens have found past exposure to this virus9,10,80, Tick-borne pathogens meanwhile, there is no information about the exposure Ticks are hematophagous ectoparasites of almost every or infection with FPV in wild species. Both CPV and terrestrial vertebrate and play an important role as vector FPV, have shown to cause gastrointestinal affections of pathogens95. In Chile, viral and bacterial tick-borne in carnivores elsewhere83, but infections and potential pathogenic agents have been neglected and information pathological consequences of these viruses on Chilean available about the presence of Anaplasma platys96, species are still undetermined. Ehrlichia canis97, “Candidatus Rickettsia andeanae”98 Like parvoviruses, information about retroviruses in and Rickettsia felis99 is restricted to domestic mammals.

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However, a recent study identified “Candidatus Neoeh- Dogs are another threat for Chilean wildlife due to rlichia chilensis” in wild rodent species from southern their predatory behaviour over native species and for Chile using molecular methods100. their role as carriers of infectious pathogens108. Dogs in- Recently, Borrelia burgdorferi was reported in Brazil, habiting natural areas have been linked with outbreaks of Mexico, Canada, Chile, Costa Rica, Colombia and Vene- viral diseases in carnivore populations that have resulted zuela101, however, most cases have been diagnosed based in mass mortality events of wild animals in the past109. only on clinical and serological evidence, without a mo- Dogs populations have increased in size and density over lecular characterization and isolation of the agent101. This the years in urban and rural areas of Chile, which might has only been done by Ivanova et al. (2014), who reported increase the possibility of encounters between wildlife Borrelia chilensis VA1, a new spirochete species from the and domestic dogs and the transmission of pathogenic Lyme group102. Additionally, Verdugo et al. (2017), found organisms10,46,78,79,110. infection with B. chilensis in Ixodes stilesi ticks collected from the native southern pudu deer and suggests that I. stilesi may be playing a role in the maintainance of the Conclusions spiroquete103. Further studies are necessary to properly understand the mechanisms of natural transmission of To date, most publications have involved the study of this bacterium and the risks of infection for domestic zoonotic viral and bacterial pathogens in Chilean wild animals and humans. mammals. Non-zoonotic and vector-borne pathogens have been neglected by the local scientific community, Pathogen transmission between wildlife and despite their importance for wildlife conservation and domestic animals public health, respectively. It is also concerning that a Pathogen transmission between wild species and lives- large number of studies have been performed in southern tock is bidirectional and affect both animal production and and central regions of Chile, while the development of species conservation all over the world104. Factors, such research studies in the northern areas of the country have as human encroachment into wildlife inhabited areas and been limited. Research about viral and bacterial pathogens the expansion and intensification of animal production in Chilean wild mammals is still very scarce and further systems to natural areas, can increase the risk for contact studies are necessary in order to properly understand the and pathogen transmission at the livestock-wildlife role that certain species might be playing as reservoir interface105. The interaction among livestock and wild of infectious agents. The information gathered in future species not only occurs in anthropogenically disturbed investigations dedicated to evaluate the presence of in- zones, but also in protected natural areas of Chile71,106. fection in wild mammals will establish the basis for more Pathogens, such as MAP, BVDV and Corynebacterium complex studies destined to understand the epidemiology pseudotuberculosis, are being transmitted from farm ani- and ecology of zoonotic and non-zoonotic infectious mals to wild ungulates facing conservation issues70,88,107. diseases in the country. For this reason, it is extremely relevant to understand the consequences that these infectious agents might have on Acknowledgments. The authors would like to thank the health of the affected species and the existent mecha- Mr. Andrés Felipe Peña for his assistance with the ma- nisms for the transmission of diseases between livestock nagement of literature references. We acknowledge the animals and wildlife. support of FONDECYT nº 1170972

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 201 Infectología al Día 39 32 33 38 38 38 37 43 38 38 41 41 36 41 36 41 113 113 113 111 112 Reference PCR PCR PCR RT/PCR RT/PCR RT/PCR RT/PCR mouse inoculation test mouse inoculation tests Diagnostic technique Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Mouse inoculation test and Direct immunofluorescence Mouse inoculation test and Direct immunofluorescence Mouse inoculation test and Mouse inoculation test and Direct immunofluorescence Mouse inoculation test and Mouse inoculation test and Mouse inoculation test and RT/PCR and DNA sequencing RT/PCR and DNA sequencing RT/PCR and DNA sequencing indirect immunofluorescence immunofluorescence and RT/ immunofluorescence and RT/ immunofluorescence and RT/ Mouse inoculation test, indirect Mouse inoculation test, indirect Mouse inoculation test, indirect Direct immunofluorescence and Direct immunofluorescence and a (2) Location Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Lagos (1) regions O’Higgins region (1) Metropolitana region Metropolitana region Metropolitana region Metropolitana region Coquimbo to Los Lagos regions Metropolitana (9), Valparaíso (2), Metropolitana (9), Valparaíso Metropolitana (260), Biobío (158), Coquimbo to Los Ríos regions From (13), Metropolitana (60), Valparaíso Araucanía (10) and Atacama regions (45), Los Lagos (44), Coquimbo (17), Coquimbo (4), Araucanía (2) and Los O’Higgins (13), Maule (8), Biobío (7), Metropolitana and Valparaíso regions Metropolitana and Valparaíso Valparaíso (88), O’Higgins (48), Maule Valparaíso (4.95%) 1 positive 1 positive 1 positive positives 4 positives 4 positives 3 positives 2 positives 2 positives 3/3 (100%) 64 positives 27 positives 82 positives Number of 1243/23868 Prevalence/ 856 positives 910 positives 297 positives 568 positives 672 positives 104 positives (percentage) 12/73 (14.1%) 1/619 (0.16%) - (AgV4) (AgV4) (AgV9) (AgV4) (AgV4) (AgV4) (AgV4) Cluster I Cluster III Cluster IV Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determinded Genetic lineage E Genetic lineage B Genetic lineage B Genetic lineage C Genetic lineage C Genetic lineage D characterization Antigenic variant 4 Antigenic variant 4 Antigenic variant 9 Antigenic variant 4 Antigenic variant 4 Antigenic variant 4 Antigenic variant 4 genic variant 4 (AgV4) Genetic lineage A Anti A Genetic lineage Host Tadarida brasiliensis Tadarida Brazilian free-tailed bat Host Order

Chiroptera

Rabies (Rhabdoviridae)

Annexed. Summary of peer-reviewed studies published from 1951 to 2017 evaluating the prevalence of bacterial and viral infections in Chilean wildlife Annexed. Summary of peer-reviewed Pathogen

202 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día 38 38 43 39 38 33 37 38 36 43 41 33 39 38 33 39 43 32 33 37 36 113 113 113 Reference PCR PCR PCR RT/PCR mouse inoculation test mouse inoculation test mouse inoculation tests mouse inoculation tests Diagnostic technique Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Mouse inoculation test and Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence RT/PCR and DNA sequencing RT/PCR and DNA sequencing RT/PCR and DNA sequencing immunofluorescence and RT/ immunofluorescence and RT/ immunofluorescence and RT/ Mouse inoculation test, indirect Mouse inoculation test, indirect Mouse inoculation test, indirect Direct immunofluorescence and Direct immunofluorescence and Direct immunofluorescence and Direct immunofluorescence and - gions Location Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Biobío region Metropolitana region Metropolitana region Metropolitana region Metropolitana (3), Valparaíso (3), Metropolitana (3), Valparaíso Metropolitana (19), Valparaíso (1), Metropolitana (19), Valparaíso Metropolitana to Los Ríos re From O’Higgins (2) and Biobío regions (5) Biobío (3) and Magallanes regions (4) 0/8 0/4 14/81 24/188 44/131 (14.74%) (11.32%) (25.14%) 1 positive 1 positive positives 9 positives 4 positives 4 positives 4 positives 5 positives 3 positives 9 positives 9 positives 52 positives 11 positives 19 positives 14 positives 27 positives 14 positives 37 positives 13 positives Number of Prevalence/ 1/7 (12.50%) (percentage) typed typed (AgV6) (AgV6) (AgV6) (AgV4) (AgV 4) (AgV6)| Cluster III Cluster IV Cluster IV Pathogen Pathogen Not specified Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Genetic lineage E Genetic lineage B Genetic lineage A Genetic lineage A characterization Antigenic variant 6 Antigenic variant 6 Antigenic variant 6 Antigenic variant 6 Antigenic variant 4 Antigenic variant 4 Antigenic variant not Antigenic variant not Host Hoary bat Lasiurus sp. Histiotus sp. Eastern Red Bat Lasiurus borealis Lasiurus cinereus Histiotus macrotus Histiotus montanus Big-eared brown bat Small big-eared brown bat

Chiroptera Chiroptera Chiroptera Chiroptera Chiroptera Chiroptera Host Order

Annexed. Continuation Pathogen

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 203 Infectología al Día 33 33 33 33 33 33 39 33 33 48 33 33 38 33 38 38 41 38 37 43 33 113 Reference PCR RT/PCR mouse inoculation tests mouse inoculation tests mouse inoculation tests mouse inoculation tests Diagnostic technique Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence Mouse inoculation test and Direct immunofluorescence Direct immunofluorescence Direct immunofluorescence RT/PCR and DNA sequencing immunofluorescence and RT/ Mouse inoculation test, indirect Direct immunofluorescence and Direct immunofluorescence and Direct immunofluorescence and Direct immunofluorescence and Location Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Not specified Lagos (2) regions Valparaíso region Valparaíso Magallanes region: Metropolitana region Metropolitana (2), Atacama (1), (1), Morro Chico (1), Porvenir (2) (1), Morro Chico Porvenir (1), Araucanía (1) and Los Valparaíso Bernardo O’Higgins (1), San Gregorio 0/3 0/1 0/2 0/1 0/4 0/3 0/3 0/8 0/5 0/1 0/120 (1.06%) 13/1210 1 positive positives 9 positives 6 positives 2 positives 7 positives 5 positives 2 positives 2 positives 2 positives Number of Prevalence/ 5/58 (8.62%) (percentage) (AgV8) (AgV3) (AgV3) (AgV4) (AgV3) Cluster II Pathogen Pathogen Not determined Not determined Not determined Not determined Genetic lineage A Genetic lineage D characterization Antigenic variant 8 Antigenic variant 3 Antigenic variant 3 Antigenic variant 4 Antigenic variant 3 Host Guiña Coypu Myotis sp. Pampas cat Pampas Galictis cuja Vampire bat Vampire Lesser grison Lycalopex sp. Lycalopex Mountain lion Otaria byronia Puma concolor Myotis chiloensis Mouse-eared bat Lycalopex griseus Lycalopex Southern Red Bat Leopardus guigna Myocastor coypus Conepatus chinga Lasiurus blossevillii Leopardus colocolo Desmodus rotundus Kalinowski’s Mastiff Bat South American sea lion South American gray fox Mormopterus kalinowskii Molina’s Hog-nosed skunk

Rodentia Carnivora Carnivora Carnivora Carnivora Carnivora Carnivora Carnivora Carnivora Chiroptera Chiroptera Chiroptera Chiroptera Chiroptera Host Order

Annexed. Continuation Pathogen

204 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día 9 79 83 79 49 57 56 53 10 59 54 52 80 50 51 50 51 10 52 59 49 54 Reference - d d d d ELISA ELISA ELISA ELISA ELISA ELISA ELISA ELISA ELISA Serology Serology Serology Serology zation test and RT-PCR Seroneutralization test Diagnostic technique Microneutralization test Microneutralization assay Microneutralization test and Microneutralization test and Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Cytopathic effect in cell culture Cytopathic effect in cell culture Indirect ELISA and seroneutrali regions Location region (1) Aysén region Aysén region Aysén region Aysén region Biobío region Biobío region Los Ríos region Los Ríos region Los Lagos region Los Lagos region Coquimbo region Coquimbo region Coquimbo region Los Lagos regions Magallanes region Metropolitana region Los Lagos and Ríos regions Metropolitana (7) and O’Higgins (1) and Metropolitana regions Metropolitana, Biobío, O’Higgins, including the Metropolitana region Araucanía, Los Lagos and Aysén (4) (1), O’Higgins Biobío (2), Valparaíso Aysén (11), O’Higgins (5), Biobío (2), Araucanía (3), Los Ríos (1), Lagos to Los Lagos regions Valparaíso From (1), Maule Araucanía, Los Ríos and Los Ríos (10) and Lagos regions (4) f e b c c 0/3 0/98 18/59 0/127 7.50% 12.7% 20/209 13/102 or 5/23 (9.57%) (21.7%) (12.74%) 1 positive positives 1/5 (20%) (13.51%) 2 positives 8/16 (50%) 24 positives 6/80 (7.5%) 2/3 (66.7%) Number of No positives 14/33 (42%) Prevalence/ 9/23 (39.1%) 5/48 (10.4%) 1/69 (1.44%) (percentage) 13/28 (46.4%) 4/547 (0,73%) Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined characterization Rat

Rice Pygmy

Host Andean fox Otaria byronia spp. Lycalopex Neovison vison American mink Lycalopex griseus Lycalopex Lycalopex culpaeus Lycalopex Abrothrix olivaceus Olive-colored akodont South American gray fox South American Sea Lion Oligoryzomys longicaudatus Long-tailed

Rodentia Rodentia Carnivora Carnivora Carnivora Carnivora Carnivora Host Order Distemper (CDV) Annexed. Continuation Pathogen Hantavirus- Andes

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 205 Infectología al Día 49 53 59 53 54 59 59 50 51 52 51 51 59 51 54 54 54 55 56 54 55 54 54 56 54 55 56 Reference d d d d d ELISA ELISA ELISA ELISA ELISA ELISA ELISA ELISA ELISA ELISA Serology Serology Serology Serology Serology ELISA and PCR ELISA and PCR ELISA and PCR Diagnostic technique Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) Strip immunoblot assay (SIA) and sequencing ELISA, RT-PCR -

Location tana regions Aysén region Aysén region Biobío region Biobío region Biobío region Lagos regions Los Ríos region Los Ríos region Los Ríos region Los Lagos region Los Lagos region Los Lagos region O’Higgins region Aysén regions (2) Los Lagos regions Metropolitan region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Coquimbo (1), Valparaíso, Coquimbo (1), Valparaíso, and Metropolitana regions Metropolitana, Araucanía and Los Ríos and Lagos regions Valparaíso and O’Higgins regions Valparaíso Maule, Biobío and Los Valparaíso, Los Ríos (4) and Lagos regions O’Higgins, Maule, Biobío Valparaíso, O’Higgins, Maule, Biobío, Valparaíso, Valparaíso, Araucanía and Metropoli Valparaíso, Los Ríos (3), Biobío (2), Araucanía and Antofagasta and Metropolitana regions g g g g g g g g 0/1 0/2 0/8 0/2 0/24 0/25 0/29 2.70% 1 positive positives 2/44 (4.6%) 4/43 (9.3%) 1/19 (5.3%) 2/61 (3.3%) 2/80 (2.5%) Number of 12/300 (4%) Prevalence/ No positives No positives No positives No positives No positives No positives No positives No positives 1/36 (2.78%) 1/57 (1.75%) 1/6 (16.66%) (percentage) 3/163 (1.84%) Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined characterization Host Degu mouse Black rat Brown rat Rattus rattus House mouse Mus musculus Octodon degus Phyllotis darwini Irenomys tarsalis Thylamys elegans Rattus norvegicus Geoxus annectens Abrothrix sanborni Abrothrix longipilis Sanborn’s akodont Long-haired akodont Pearson’s long-clawed Pearson’s Chilean climbing mouse Loxodontomys micropus Darwin’s leaf-eared mouse Darwin’s leaf-eared Southern big-eared mouse Elegant Fat-tailed opossum Fat-tailed Elegant -

phia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Host Order Didelphimor Annexed. Continuation Pathogen

206 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día 9 80 89 55 10 90 89 90 91 88 88 85 85 90 114 Reference - - PCR cing cing test (HAI) test (HAI) Not specified DNA sequencing inhibition test (HAI) Diagnostic technique Visual inspection of lesions Visual inspection of lesions Visual inspection of lesions Visual inspection of lesions Hemagglutination inhibition reverse-transcriptase PCR and Haemagglutination inhibition Serological neutralization test Serological neutralization test Serological neutralization test ELISA and haemagglutination Serological neutralization test, PCR amplification and sequen PCR amplification and sequen Location Aysén region Aysén region Not specified Biobío region Biobío region Isla de Choros Los Ríos region Punta de Choros Punta de Choros Coquimbo region (O’Higgins region) (Coquimbo region) (Coquimbo region) (Coquimbo region) Chilean Northern Patagonia Los Cipreses National Reserve Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) 0/18 1 positive positives 3/4 (75%) 1 negative 2 positives 3/15 (20%) 3/3 (100%) 3/3 (100%) 1/1 (100%) Number of 16/33 (49%) Prevalence/ 1/16 (6.25%) 4/13 (30.8%) 2/15 (13.3%) 2/18 (11.1%) (percentage) 4/28 (14.29%) Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined characterization Host Guigna Guigna Brown rat Pudu puda Pudu puda Andean fox Darwin’s fox Otaria byronia Black Porpoise Lycalopex spp. Lycalopex Southern Pudu Southern Pudu Chilean Huemul Chilean Huemul Chilean Dolphin Rattus norvegicus Leopardus guigna Lycalopex fulvipes Lycalopex Leopardus guigna Tursiops truncatus Tursiops Lycalopex culpaeus Lycalopex Phocoena spinipinnis Bottle-nosed Dolphin Hippocamelus bisulcus Hippocamelus bisulcus South American Sea Lion Cephalorhynchus eutropia Rodentia Carnivora Carnivora Carnivora Carnivora Carnivora Carnivora Host Order Cetartiodactyla Cetartiodactyla Cetartiodactyla Cetartiodactyla Cetartiodactyla Cetartiodactyla Cetartiodactyla

- )

Poxvirus Feline Feline leukemia virus (FeLV) Foot-and- mouth disea Canine parvovirus (CPV) Bovine rhinotracheitis (BoHV-1) Hantavirus - Seoul Bovine viral diarrhea virus (BVDV) Tattoo skin Tattoo virus ( Feline immuno- Feline Herpesvirus (Gamma- herpesvirus) Annexed. Continuation Pathogen deficiency virus (FIV) se virus

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 207 Infectología al Día 23 24 20 19 23 24 18 28 27 20 25 26 18 17 17 25 Reference h h PCR PCR (MAT) staining staining microscopy Nested PCR Nested PCR Renal biopsy restriction enzyme (MAT) and renal biopsy (MAT) (MAT) and renal biopsy (MAT) and immunoperoxidase and immunoperoxidase Diagnostic technique agglutination test (MAT) agglutination test (MAT) microscopy and Levaditi’s microscopy and Levaditi’s Bacterial culture, dark-field Serology, immunochemical Serology, Serology, immunochemical Serology, diagnostic and microscopic diagnostic and microscopic Indirect immunofluorescence Indirect immunofluorescence Indirect immunofluorescence, Indirect immunofluorescence, immunoperoxidase, dark-field immunoperoxidase, dark-field microscopy and endonuclease Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Bacterial culture and dark-field Location regions (16) Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Los Ríos (5), Lagos (10) and Aysén 0/9 13/22 91/206 62/126 87/175 21/187 (44.2%) (49.2%) (49,7%) (59.09%) (11.23%) positives 3 positives 1/10 (10%) Number of Prevalence/ 8/14 (57.1%) 9/16 (56.3%) 6/53 (11.3%) 26/260 (10%) (percentage) 35/83 (42.2%) 19/41 (46.3%) 7/144 (4.86%) 31/57 (55.6%) Serovar Pathogen Pathogen Serovar Poi (3) Serovar Poi (1), Hardjo Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined (1), Medanensis (3), Copenhageni Serovar Sejroe (5), characterization Hardjo (3), Pomona Hardjo (3), Pomona (2), Medanensis (1), Poi (2) Copenhageni Poi Icterohaemorrhagiae Icterohaemorrhagiae Icterohaemorrhagiae- Medanensis (1), Sejroe Copenhageni, Pomona, Copenhageni, Pomona, Icterohaemorrhagiae (1), Host Degu Neovison vison American mink Octodon degus Abrothrix longipilis Abrothrix olivaceus Long-haired akodont Olive-colored akodont

Rodentia Rodentia Rodentia Carnivora Host Order

spp. Annexed. Continuation Pathogen Leptospira

208 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día 19 27 18 24 18 25 24 23 17 17 25 23 20 26 18 20 115 116 Reference h h PCR PCR (MAT) staining staining microscopy Nested PCR Nested PCR Nested PCR Renal biopsy restriction enzyme (MAT) and renal biopsy (MAT) (MAT) and renal biopsy (MAT) and immunoperoxidase and immunoperoxidase Diagnostic technique Guineae pig inoculation agglutination test (MAT) agglutination test (MAT) microscopy and Levaditi’s microscopy and Levaditi’s Bacterial culture, dark field Serology, immunochemical Serology, Serology, immunochemical Serology, diagnostic and microscopic diagnostic and microscopic Indirect immunofluorescence Indirect immunofluorescence Indirect immunofluorescence, Indirect immunofluorescence, immunoperoxidase, dark-field immunoperoxidase, dark-field microscopy and endonuclease Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Bacterial culture and dark-field Location Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region 0/15 77/191 51/246 (40.3%) (20.7%) positives 3/5 (60%) 2 positives 2 positives 3/62 (4.8%) 4/68 (5.9%) Number of Prevalence/ 2/45 (4.44%) 9/34 (26.5%) 7/17 (41.8%) 1/3 (33.33%) 5/84 (5.95%) (percentage) 18/85 (21.2%) 16/76 (21.1%) 25/89 (28.1%) 15/36 (41.7%) 15/36 (41.7%) - - - rrhagiae rrhagiae Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined characterization Medanensis, Hardjo Icterohaemorrhagiae Hardjo, Pomona, Poi, Poi, Hardjo, Pomona, Serovar Copenhageni Serovar Icterohaemo Serovar Icterohaemo Icterohaemorrhagiae- hageni-Poi (1), Sejroe, hageni-Poi Medanensis (1), Sejroe, (2), Poi (3), Pomona (3), (3), Pomona (2), Poi Copenhageni (1), Copen Serovar Copenhageni (1),

Rat

Rice Pygmy

Host Black rat Rattus sp. Rattus rattus Phyllotis darwini Darwin’s pericote Oligoryzomys longicaudatus Long-tailed Host Order

Rodentia

Rodentia Rodentia

Rodentia Annexed. Continuation Pathogen

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 209 Infectología al Día 24 23 24 24 25 18 20 25 18 23 24 26 17 17 26 17 25 14 116 116 Reference - h h h h PCR PCR (MAT) staining staining croscope Nested PCR Nested PCR restriction enzyme restriction enzyme (MAT) and renal biopsy (MAT) and immunoperoxidase and immunoperoxidase and immunoperoxidase and immunoperoxidase Diagnostic technique agglutination test (MAT) agglutination test (MAT) agglutination test (MAT) agglutination test (MAT) microscopy and Levaditi’s microscopy and Levaditi’s Bacterial culture, dark-field Bacterial culture, dark-field Serology, immunochemical Serology, Serology, immunochemical Serology, Serology, immunochemical Serology, Serology, immunochemical Serology, diagnostic and microscopic diagnostic and microscopic diagnostic and microscopic diagnostic and microscopic Indirect immunofluorescence Indirect immunofluorescence Indirect immunofluorescence Indirect immunofluorescence Indirect immunofluorescence, Indirect immunofluorescence, immunoperoxidase, dark-field immunoperoxidase, dark-field microscopy and endonuclease microscopy and endonuclease Microscopic agglutination test Microscopic agglutination test Direct observation with ultrami Microscopic agglutination test (MAT) Location Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Metropolitan region Metropolitana region Metropolitana region Metropolitana region Metropolitan region 0/1 0/2 0/1 0/1 0/8 0/2 0/13 positives 1/2 (50%) 2/26 (7.7%) 1/8 (12.5%) 3/9 (33.3%) Number of 2/27 (7.4%) Prevalence/ 6/47 (12.8%) 2/14 (14.3%) 3/29 (10.3%) 63/100 (63%) (percentage) 20/97 (20.6%) 24/63 (38.1%) 7/31 (22.58%) 18/80 (22.5%) Serovar Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined characterization Icterohaemorrhagiae Host Brown rat House mouse Mus musculus Rattus norvegicus Geoxus valdivianus Loxodontomys micropus Long-clawed mole mouse Southern big-eared mouse Host Order

Rodentia

Rodentia Rodentia

Rodentia

Annexed. Continuation Pathogen

210 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día 9 27 21 27 18 21 27 28 22 22 22 22 22 21 22 21 22 21 21 21 Reference ------

d 4 d d d d d cing (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) rial culture rial culture rial culture rial culture rial culture rial culture Nested PCR (MAT) and PCR (MAT) bacterial culture Serology, microscopy or Serology, Diagnostic technique Immunohistochemestry (IHC) Ribosomal RNA gene sequen Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Serology, microscopy or bacte Serology, Serology, microscopy or bacte Serology, Serology, microscopy or bacte Serology, Serology, microscopy or bacte Serology, Serology, microscopy or bacte Serology, Serology, microscopy or bacte Serology, Location Aysén region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Metropolitan region Metropolitana region Metropolitana region Metropolitana region j i 0/8 0/9 0/2 0/7 0/1 0/4 0/68 0/68 positives 1/4 (25%) 5 positives 1/1 (100%) 5/7 (71.4%) 4/7 (57.1%) Number of Prevalence/ 7/144 (4.9%) 1/3 (33.33%) 8/31 (25.8%) 26/260 (10%) (percentage) 29/60 (48.3%) 12/53 (22.6%) 12/33 (36.4%) - - - - - hageae Pathogen Pathogen Not determined Not determined Not determined Not determined Not determined Not determined geae (1), Pomona characterization Hardjo (2), Canicola Pomona (1), Hardjo, Pomona Hardjo (2), Javanica, na, Hardjo, Canicola (7), Serovar Pomona (3), Serovar Pomona Serovar Bratislava (2) Icterohaemorrhageae Icterohaemorrhagiae, Serovar Bratislava and Copenhageni, Canicola (1), Hardjo-Pomona (2), (1), Hardjo-Pomona Serovar Hardjo (1), Java Canicola, Icterohaemorr nica (5), Icterohaemorra geae-Javanica (1), Pomo Serovar Icterohaemorrha

Rat

Rice Pygmy

Host Degu Black rat Brown rat Rattus rattus House mouse Mus musculus Otaria byronia Neovison vison American mink Octodon degus Phyllotis darwini Phyllotis darwini Darwin’s pericote Darwin’s pericote Rattus norvegicus Abrothrix longipilis Geoxus valdivianus Abrothrix olivaceus Long-haired akodont Olive-colored akodont South American Sea Lion Long-clawed mole mouse Oligoryzomys longicaudatus Long-tailed Host Order Rodentia

Rodentia Rodentia Carnivora Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Carnivora

Annexed. Continuation Pathogen Leptospira interrogans

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 211 Infectología al Día 9 9 27 27 27 27 28 72 73 70 27 27 27 27 73 66 68 69 67 65 117 117 117 117 Reference -

cing (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) (MAT) and PCR Histopathology Histopathology Histopathology culture and PCR Bacterial culture Bacterial culture Bacterial culture Bacterial culture and real-time PCR Diagnostic technique Histopathology, bacterial Histopathology, Bacterial culture and PCR Immunohistochemestry (IHC) Immunohistochemestry (IHC) Ribosomal RNA gene sequen Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Microscopic agglutination test Mycobacteria growth indicator Mycobacteria detection system Mycobacteria detection system tube (MGIT) and Real-time PCR Bacterial culture and Real-time PCR Location regions (1) Biobío region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Lagos region Magallanes region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Metropolitana region Aysén and Magallanes regions Los Ríos and Lagos regions Los Ríos and Lagos regions (Bernardo O’Higgins National Park) Los Ríos (2), Lagos (1) and Aysén i 0/3 0/68 0/68 0/68 0/68 0/260 0/260 0/260 48/380 (12.6%) positives 4 positives 3/15 (20%) 9/9 (100%) 4/4 (100%) 3/3 (100%) 1/1 (100%) Number of Prevalence/ 5/32 (15.6%) 2/106 (1.9%) 2/117 (1.7%) 2/3 (66.67%) 6/14 (42.8%) 14/14 (100%) (percentage) 2/260 (0.77%) 62/92 (67.4%) 21/501 (4.2%) Pathogen Pathogen Serovar Patoc Serovar Ballum Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined characterization Serovar Grippotyphosa Rat

Rice Pygmy

Host Degu Degu Degu Degu Red deer Guanaco Brown rat Pudu puda Fallow deer Fallow (Dama dama) Otaria byronia Otaria byronia European hare Neovison vison Southern Pudu Cervus elaphus American mink Lama guanicoe Octodon degus Octodon degus Octodon degus Octodon degus Chilean huemul Phyllotis darwini Phyllotis darwini Phyllotis darwini Phyllotis darwini Lepus europaeus Darwin’s pericote Darwin’s pericote Darwin’s pericote Darwin’s pericote Rattus norvegicus Abrothrix longipilis Abrothrix olivaceus Long-haired akodont Olive-colored akodont (Hippocamelus bisulcus) South American Sea Lion South American Sea Lion Oligoryzomys longicaudatus Long-tailed Host Order Rodentia Rodentia Carnivora Carnivora Carnivora Rodentia Cetartiodactyla Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Rodentia Lagomorpha Cetartiodactyla Cetartiodactyla Cetartiodactyla Cetartiodactyla para- Annexed. Continuation Pathogen Leptospira borgpetersenii Leptospira kirschneri Leptospira biflexa Leptospira santarosai Yersinia enterocolitica Mycobacterium avium tuberculosis

212 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día 9 9 9 89 118 103 118 118 118 118 100 100 118 118 119 Reference - quencing sequencing Bengal rose RReal-time PCR RReal-time PCR RReal-time PCR Rose Bengal test DNA sequencing DNA sequencing detection by PCR Plaque agglutination Plaque agglutination Real-time PCR and DNA Diagnostic technique cPCR and DNA sequencing cPCR and DNA sequencing PPCR and DNA sequencing Real-time PCR and DNA se Bacterial culture and invA gene Location Aysén region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Antofagasta region Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) Chiloé Island (Los Lagos region) i i 0/3 0/3 0/3 0/2 0/18 1/30 0/30 0/30 0/30 17/30 (3.3%) (56.67%) 1 positive positives 4/5 (80%) 1/5 (20%) 8 positives Number of Prevalence/ (percentage) 2/13 (15.38%) Pathogen Pathogen Newport (1) Not determined Not determined Not determined Not determined characterization Serovar Havana (1), Host Pudu puda Darwin’s fox Darwin’s fox Darwin’s fox Darwin’s fox Darwin’s fox Darwin’s fox Darwin’s fox Abrothrix sp. House Mouse Mus musculus Otaria byronia Otaria byronia Otaria byronia Otaria byronia Southern Pudu Chilean Huemul Lycalopex fulvipes Lycalopex Lycalopex fulvipes Lycalopex fulvipes Lycalopex fulvipes Lycalopex Lycalopex fulvipes Lycalopex Lycalopex fulvipes Lycalopex Lycalopex fulvipes Lycalopex Hippocamelus bisulcus South American Sea Lion South American Sea Lion South American Sea Lion South American Sea Lion Host Order Cetartiodactyla Carnivora Carnivora Carnivora Carnivora Rodentia Carnivora Carnivora Carnivora Rodentia Carnivora Carnivora Carnivora Cetartiodactyla Carnivora sp. sp. sp. sp.

Annexed. Continuation Pathogen Mycoplasma sp. Mycoplasma haemocanis Mycoplasma haemofelis Coxiella burnetti Borrelia Bartonella Rickettsia Candidatus Neoehrlichia chilensis Salmonella enterica Brucella Brucella canis Brucella abortus

Rev Chilena Infectol 2019; 36 (2): 195-218 www.revinf.cl 213 Infectología al Día

107 123 138 138 137 138 138 121 137 137 122 120 the same Reference confirmed in The study specified the collection e analysis Bacterial culture Bacterial culture Bacterial culture Bacterial culture Bacterial culture Bacterial culture Bacterial culture Bacterial culture Bacterial culture Diagnostic technique Bacterial culture and PCR Bacterial culture and PCR Only the prevalence is indicated but there c Bacterial culture and amplified performed in samples fragment length polymorphism The study does not indicate if each fecal sample collected was fromwas collected sample fecal each if indicate not does study The k DNA/RNA sequencing was The total number of individuals examined in the study was not specifiedwas not study the in individuals examined of number total The i g Location Aysén region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Los Ríos region Tarapacá region Tarapacá Coquimbo region Coquimbo region Coquimbo region Coquimbo region Coquimbo region (6.7%) (73.3%) l k (6.7%) k positives 1/5 2/2 (100%) 1/30 (3.3%) 2/30 (6.7%) 2/30 (6.7%) 4/53 (7.5%) 2/53 (3.8%) 1/53 (1.9%) 1/53 (1.9%) Number of 1/15 Prevalence/ (percentage) 13/53 (24.5%) 22/30 The study does not indicate if each sample was collected from a unique individual. l The specific serological method for analysis was not indicated in the study. The specific serological method for analysis was not indicated in the study. d - - ization Strain OFI Ovine genotype Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined Not determined DAEC (Diffusely- pathogenic E. coli ) adherent Escherichia coli ) (1), EPEC (Entero Pathogen character Pathogen 9 seropositive samples considering a titer cut-off of 1:8 and 5 positives with 1:16. b Host Otaria byronia Otaria byronia Otaria byronia Otaria byronia Otaria byronia Otaria byronia Chilean Huemul Chinchilla lanigera Chinchilla lanigera Chinchilla lanigera Chinchilla lanigera Chinchilla lanigera Long-tailed chinchilla Long-tailed chinchilla Long-tailed chinchilla Long-tailed chinchilla Long-tailed chinchilla Hippocamelus bisulcus South American Sea Lion South American Sea Lion South American Sea Lion South American Sea Lion South American Sea Lion South American Sea Lion Only the number of captured individuals is specified not the number of analyzed samples. samples. analyzed of number the not specified is individuals captured of the number Only f The specific serological and immunohistochemical method for analysis were not indicated in the study. The specific serological and immunohistochemical method for analysis were not indicated in the study. h Host Order Carnivora Carnivora Carnivora Carnivora Rodentia Carnivora Cetartiodactyla Carnivora Rodentia Rodentia Rodentia Rodentia The detail of number of positive samples presented in this study does not match with the total number of positive samples. samples. positive of number total the with match not does study this in presented samples positive of number of detail The j Regions were not specified for each positive sample. in the methodology. in the methodology. a unique individual or samples were taken more than one time from the same individual. Annexed. Continuation Pathogen a no information about number of positive cases nor total individuals studied. study. study. Escherichia coli Campylobacter insulaenigrae Edwarsiella tarda Klebsiella pneumoniae Proteus mirabilis Corynebacterium pseudo- tuberculosis Morganella morganii Staphylococcus aureus Pseudomona auriginosa samples. only 14 positive site for

214 www.revinf.cl Rev Chilena Infectol 2019; 36 (2): 195-218 Infectología al Día

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