Recommendations for Infectious Disease Screening in Migrants to Western Europe with Inflammatory Arthropathies Before Starting Biologic Agents

Recommendations for infectious disease screening in migrants to Western Europe with inflammatory arthropathies before starting biologic agents. Results from a multidisciplinary task force of four European societies (SIR, SER, SIMET, SEMTSI) facing the largest impact of the flow of migrants today F. Bartalesi1, C.A. Scirè2, A. Requena-Méndez3, M.A. Abad4, D. Buonfrate5, R. Caporali6, F. Conti7, F. Diaz-Gonzalez8, C. Fernández-Espartero9, C. Martinez-Fernandez10, M. Mascarello11, E. Generali12, G. Minisola12, A. Morrone13, J. Muñoz3, P. Richi14, G. Sakellariou6, J. Salas Coronas14, M. Spinicci1, F. Castelli15, A. Bartoloni1, Z. Bisoffi5, F. Gimenez-Sanchez16, S. Muñoz Fernández14, M. Matucci-Cerinic17 1SOD Malattie Infettive e Tropicali, Careggi Hospital, Florence, Italy; 2Rheumatology Unit, Dept. of Medical Sciences, University of Ferrara, and Epidemiology Unit, Italian Society for Rheumatology, Milano, Italy; 3Barcelona Institute for Global Health (ISGlobal-CRESIB), Hospital Clínic, Universitat de Barcelona, Spain; 4Division of Rheumatology, Hospital Virgen del Puerto, Plasencia, Spain; 5Centre for Tropical Diseases, Sacro Cuore Hospital, Negrar, Verona, Italy; 6Division of Rheumatology, University of Pavia, IRCCS S. Matteo Foundation, Pavia, Italy; 7Dept. of Internal Medicine and Medical Specialties, Rheumatology Unit, Sapienza University, Rome, Italy; 8Dept. of Medicine, Universidad de La Laguna, Division of Rheumatology, Hospital Universitario de Canarias, La Laguna, Spain; 9Servicio de Reumatologia, Hospital Universitario de Mostoles, Madrid; 10Research Unit, Spanish Society of Rheumatology, Madrid, Spain; 11Infectious Diseases Unit, University Hopital of Trieste, Italy; 12Division of Rheumatology, San Camillo Hospital, Rome, Italy; 13General Directorate, San Camillo Hospital, Rome, Italy; 14Division of Rheumatology, Hospital Universitario Infanta Sofía, Universidad Europea de Madrid, Spain; 15University Department of Infectious and Tropical Diseases, University of Brescia and Brescia Spedali Civili General Hospital, Italy; 16Unidad de Vacunación Internacional, Instituto Hispalense de Pediatría, Granada, Spain, Spanish Society of Tropical Medicine and International Health; 17Dept. of Experimental and Clinical Medicine, Div. Rheumatology AOUC, University of Florence, Italy. Abstract Objective Inflammatory arthritis needs infectious disease screening before starting a biologic agent, however, few data are known about migrant patients, who represent a peculiar population which requires a multidisciplinary approach among international health specialists and should also be considered by health authorities. For this reason, the Italian and Spanish Societies of Rheumatology (SIR and SER) and Tropical Medicine (SIMET and SEMTSI) promoted a multidisciplinary task force in order to produce specific recommendations about screening and advices to be considered in migrant patients with inflammatory arthritis candidate to receive biological therapy, according to their geographical origin.

Methods The experts provided a prioritised list of research questions and the eligible spectrum of inflammatory arthritis, biologic drugs and infectious disease were defined in order to perform a systematic literature review. A search was made in Medline, Embase and Cochrane library, updated to March 2015. Ubiquitous infections and HBV, HCV, HIV and tuberculosis that are already considered in national and international recommendations, were not included. The strength of each recommendation was determined.

Results The task force members agreed on 7 overarching principles. The risk of reactivation of selected potentially latent infectious disease was addressed in migrants with inflammatory arthritis candidates for biologics was considered and 15 potentially relevant infections were identified.

Conclusion Fifteen disease-specific recommendations were formulated on the basis of high level of agreement among the experts panel.

Key words rheumatoid arthritis, psoriatic arthritis, ankylosing spondylitis, anti-TNF, infections, systematic review

Clinical and Experimental Rheumatology 2017 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

Filippo Bartalesi, Carlo A. Scirè, Introduction reactivation of unusual infections, for Ana Requena-Méndez, Miguel Angel Abad, The use of biological agents has grown which screening is not routinely pro- Dora Buonfrate, Roberto Caporali, exponentially in rheumatology and vided, has been reported (4). Fabrizio Conti, Federico Diaz-Gonzalez, other specialties. In rheumatic dis- The correct management of patients Cruz Fernández-Espartero, Carmen Martinez-Fernandez, eases, biological treatments have been coming from endemic areas for endem- Marta Mascarello, Elena Generali, largely used in inflammatory arthriti- ic, tropical and/or neglected disease Giovanni Minisola, Aldo Morrone, des (IA) such as rheumatoid arthritis who undergo biological treatment is a Jose Muñoz, Patricia Richi, (RA), psoriatic arthritis (PsA) and an- problem, which deserves consideration Gariffalia Sakellariou, Joaquin Salas kylosing spondylitis (AS), contributing by rheumatologists. While in these cas- Coronas, Michele Spinicci, to control disease progression and im- es a global work up of several diseases Francesco Castelli, Alessandro Bartoloni, proving patients’ quality of life. Their is not feasible, screening strategies and Zeno Bisoffi, Francisco Gimenez-Sanchez, Santiago Muñoz Fernández, use has revealed an increased risk of clinical monitoring can be personalised Marco Matucci-Cerinic serious adverse events, fostering new according to the region of origin. Please address correspondence to: infectious events and, mostly, reactiva- In this regard, in accordance with the Marco Matucci-Cerinic, MD, PhD, tion of chronic/latent infectious diseas- new concept of global health, a multi- Division of Rheumatology, es (1). Granulomatous infections are disciplinary approach among interna- Department of Experimental widely documented in patients treated tional health specialists is a fundamen- and Clinical Medicine, with biological agents, especially anti- tal but there is still the unmet need to Villa Monna Tessa, TNF-α inhibitors, thus suggesting a approach problems in migrant patients Viale Pieraccini 18, class effect (2). For this reason, screen- that health authorities should consider. 50139 Firenze, Italy. E-mail: [email protected] ing for active and latent chronic infec- For this reason, the Italian and Spanish Received on November 11, 2016; accepted tious diseases in patients who are can- Societies of Rheumatology (SIR and in revised form on January 23, 2017. didates for biological agents is manda- SER) and Tropical Medicine (SIMET tory. In developed countries, screening and SEMTSI) promoted a multidis- © Copyright Clinical and Experimental Rheumatology 2017. for infectious diseases is generally lim- ciplinary task force in order to pro- ited to chronic viral hepatitis and latent duce specific recommendations about tuberculosis infection (LTBI). screening and advices to be considered Increasing globalisation and the re- in migrant patients with IA candidate to markable number of migrating and receive biological therapy, according travelling people worldwide makes this to their geographical origin. This aim approach no longer adequate. Migra- was achieved following standard oper- tion between different epidemiological ating procedures, combining available environments causes new challenges to evidence from medical literature with health systems, which must be taken in expert opinion (5). Our recommenda- account to ensure equitable access to tions target all physicians and nurses care and an early identification of the who are involved in the care for pa- various threats, risks and challenges tients with IA. of the migrant populations (3). In this framework, the new concept of global Materials and methods health is defined as ‘health without Expert committee borders’, to interpret and examine The committee consisted of 11 rheuma- the relationship between people and tologists, 10 tropical/infectious disease countries, based on globalisation and physicians, and 3 clinical epidemiolo- its impact on health. For this reason, gists, representing two European coun- new health-promotion programmes tries (Italy and Spain) that are currently and screening strategies for the preven- facing the largest wave of migrants. tion and control of infectious diseases are needed today, particularly because Definitions the reactivation of neglected latent in- In these recommendations, the term fections, due to underlying conditions, ‘migrant’ refers to people from coun- such as HIV infection, haematological tries/areas with negative net migration malignancies, solid-organ transplanta- index (Central/South America, Asia, Af- tion or immunosuppressive therapies, rica, Eastern Europe), migrated to West- Funding: this study received unrestricted may often result in severe and some- ern Europe (WE). WE was defined in funding from the Italian Society for times life-threatening manifestations accordance to United Nations Regional Rheumatology. and complications. Also, in the context Groups definition. IA include RA, PsA, Competing interests: none declared. of treatment with biological agents, AS and undifferentiated arthritides.

2 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

Biologic drugs include anti-TNF-α Table I. Evidence categories and strength of recommendations. (infliximab, etanercept, adalimumab, Category Evidence certolizumab pegol, golimumab), anti- CD20 (rituximab), anti-CTLA4 (abata- Ia Meta-analysis of randomised controlled trials cept), anti-IL6 (tocilizumab), anti-IL1 Ib Randomised controlled trial (anakinra). II Prospective controlled intervention study without randomisation III Descriptive/analytic study (including case-control, cross-sectional, case series) Latent infections are defined as -per IV Expert committee reports or opinion or clinical experience of respected authorities or both sistent infections that remain silent for a period of time and reactivate in the Strength Based on presence of immune disorders (oppor- A Category I evidence tunistic infections), despite being able B Category II evidence or extrapolated recommendations from category I evidence to cause symptomatic infections also in C Category III evidence or extrapolated recommendations from category I or II evidence immunocompetent hosts. D Category IV evidence or extrapolated recommendations from category II or III evidence

Development of recommendations Table II. List of latent infection considered by the panel of expert for recommendation. A preliminary search looked for evidence on the risk of infection between Disease Screening Candidates for screening Available tests non-WE regions versus WE regions, Mycobacterial diseases with a special focus on countries with a Hansen’s diseases No None negative migration index. For this pur- Non-TB mycobacteria No None § pose, official sources were preliminary MDR-TB Yes All patients TST/IGRAs searched, and when no sufficient evi- Bacterials diseases dence was retrievable, ad hoc searches Brucellosis No Serology Salmonellosis Yes Patients from highly endemic areas Stool and urine cultures of systematic reviews or primary stud- (typhi/paratyphi) with cholelithiasis/urinary tract defect ies were done. A world map of 20 geographical regions with relative preva- Parasitic diseases Leishmaniasis No Serology, PCR lence of each infection was drawn us- Babesiosis No Blood smears, serology, ing WE-prevalence as the denominator. PCR These data enabled the expert panel to Strongyloidiasis Yes Migrants from endemic areas and Serology and stool test if select the relevant infections to be in- autochthonous patients with eosinophilia available Cysticercosis No Serology cluded in the systematic searches. Chagas disease Yes Patients from/whose mother was born Serology The experts were invited to define the in/blood transfused in endemic area coverage of the recommendations in- Viral diseases cluding diseases, drugs, and infections, HEV No Serology, PCR which were to be used as search terms HTLV-1 No Serology, PCR for the systematic literature review. Fungal diseases At the end of the first task force meet- Histoplasmosis Yes Patients from endemic areas with Serology ing, 59 potentially relevant infections suggestive history/radiological signs were identified and clinical questions Coccidioidomycosis Yes Patients from endemic areas and Serology were composed for the systematic lit- compatible clinical symptoms/history Paracoccidioidomycosis No Serology erature reviews, according to a pre- specified protocol. n.a.: not applicable; TB: tuberculosis; MDR-TB: Multi drug resistant-TB; TST: Tuberculin skin test; Medline (via PubMed), Embase, IGRA: Interferon gamma release assay. § Cochrane Central were searched un- : not specific screening for MDR-TB; same screening applied for Latent Tuberculosis Infection. til March 2015. As search terms, the MESH/Emtree terms for the defined together with proposals for recommen- The recommendations summarised in IA, biologic drugs and selected infec- dations. this article represent a consensus of tions were combined (Appendices). After examining the results of the lit- published evidence and expert opin- Only articles in English and concerning erature search, the expert panel defined ions. For each recommendation we patients aged >16 years were included. a list of potential interesting pathogens used a widely-accepted hierarchy for Other papers that were considered to be included in the recommendations. categorising the available evidence relevant in the opinion of the experts HBV, HCV, HIV and TB (except for and the strength of the recommenda- could be added. The results of the sys- multi-drug resistant TB due to the com- tions (evidence categories A–D) (Table tematic literature review (performed in plexity of its management), already I). Overarching principles and specific duplicate by CAS, GS, MM, DB, JSC, taken into account in several national recommendations were separately vot- MAA, ARM, CFE) were sent to the and international recommendations, ed and scored from 0 (no agreement committee before the second meeting, were excluded. with) to 10 (maximal agreement). The

3 Recommendations for infectious disease screening in migrants / F. Bartalesi et al. means and standard deviation (SD) of of effective eradication or prophy- Recommendation 1 the scores were calculated to determine lactic treatments before starting bio- Hansen’s disease (leprosy) should be the level of agreement among the ex- logic therapy. ruled out in patients coming from high perts panel for each recommendation. E. When appropriate screening for prevalence countries and presenting latent infections is not available, unexplained cutaneous lesions or signs Results tropical/infectious disease specialist of peripheral neuropathy; biopsies Fifteen potentially relevant infections advice should be sought to evaluate of any suspicious skin lesion should were identified (Table II). the risk-benefit ratio of starting im- be performed before starting biologi- The task force members agreed on 7 munomodulatory treatment and to cal treatment. (grade of evidence III; overarching principles and 15 disease- set up suitable clinical monitoring. strength of recommendation D; agree- specific recommendations, reaching a F. In migrant patients with IA, vaccina- ment (SD) 9.69 (0.48)) high level of agreement among the ex- tion should be performed according perts panel (Table III). to the national recommendations of Non-tuberculous mycobacteria For every considered pathogen we pre- the country where the patient should (NTM) sent briefly the disease, along with the be treated. Vaccination should be NTM include about 100 different spe- available evidence of reactivation in completed before starting biological cies of mycobacteria omnipresent in immunocompromised patients, with treatment. the environment. The geographical particular reference to IA patients ongo- G. In patients with IA who have already distribution of NTM species differs ing biological treatment. Epidemiologi- started a biologic treatmen the risk strongly worldwide and it may deter- cal data are summarised in Table IV. of infection reactivation should be mine, in part, a different burden and considered by a tropical/infectious outcome of NTM disease in each re- Statements disease specialist according to the gion (13). Each recommendation is followed in country-specific potential exposure. NTM might cause opportunistic diseas- brackets by the grade of the evidence es in condition of immunosuppression and the strength of the recommenda- Disease-specific recommendations and they are an increasingly recognised tion. • Hansen’s disease problem in the setting of IA patients Mycobacterium leprae causes a chron- on biologics and in particular on anti- Overarching principles ic granulomatous disease with highly TNF. Multiple species, both with high The Committee considered that some as- variable clinical presentations, rang- (M. marinum, M. xenopi, M. szulgai, pects related to the screening of migrant ing from skin lesions to severe damage M. kansasii, M. mucogenicum) and low people and treatment of IA might form to nerves and other organs, including (M. fortuitum, M. peregrinum, M. hae- a framework on which specific recom- bones and joints. The disease is still mophilum, M. chelonae) pathogenicity mendations could be based. These items endemic in all countries of the African have been reported in patients on bio- were therefore considered to constitute and South-East Asia regions and in logic therapy, both with anti-TNF and overarching principles, although they most countries of the Americas, West- tocilizumab (14-44). Recently, NTM were discussed and voted on. ern Pacific and Eastern Mediterranean pulmonary infections in patients with A. Migrants (included those who are Region (6). RA treated with biologic agents in Ja- considered by authorities illegal im- In IA patients on biologics, several cases pan showed that M. avium complex migrants that do not have work per- of leprosy have been reported, often with was the most frequent, followed by M. mits and residence) should be sub- a relatively shorter time of progression. gordonae. Clinical manifestations of mitted to the standard check-up and Infliximab has been associated with 2 the infection vary widely, besides pul- screening applied to all candidates cases of leprosy (7, 8), both the cases monary manifestations, also skin and for biologics. were reported in South America. Both soft tissue infection, infectious teno- B. Before starting biologics, the indi- treatments were stopped and proper synovitis, septic arthritis, lymphadeni- vidual risk of infectious diseases antimicrobial therapy was started with tis, psoas muscle abscesses, spondylo- should be estimated on the basis of resolution of the infection. Moreover, discitis, endophthalmitis and hepatitis the epidemiological risk linked to the two cases have been reported in patients have been reported. Infections have country of origin of the patient treated with etanercept (9, 10), one with been fatal in some cases. Nationality C. When a specific infectious disease adalimumab (11), and one with tocili- was available for few studies, and pa- risk is identified, an appropriate zumab (12). One patient treated with tients were from South Central USA, screening should be performed, if etanercept was previously treated with Netherlands, South Korea and Japan. available. infliximab. In one case, leprosy was A recent study reported an incidence of D. If a latent infection is suspected or defined as paucibacillary (less than 5 le- NTM infection in RA treated with anti- diagnosed, the patient should be sions), biologic treatment was stopped TNF of 0.4 x 1000 person years, while referred to a tropical/infectious dis- and then restarted after 3 months of an- another study based in USA identified eases specialist to exclude active dis- tileprosy treatment. One patient that de- 211 cases of NTM, that were more like- ease and to consider the availability veloped leprosy was from Greece. ly to live in urban settings, have pul-

4 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

Table III. Overarching principles and disease-specific recommendations: level of agreement among the experts panel.

Overarching principles

A. Migrants (included those who are considered by authorities illegal immigrants that do not have work permits and residence) should be submitted to the standard check-up and screening applied to all candidates for biologics. B. Before starting biologics, the individual risk of infectious diseases should be estimated on the basis of the epidemiological risk linked to the country of origin of the patient. C. When a specific infectious disease risk is identified, an appropriate screening should be performed, if available. D. If a latent infection is suspected or diagnosed, the patient should be referred to a tropical/infectious diseases specialist to exclude active disease and to consider the availability of effective eradication or prophylactic treatments before starting biologic therapy. E. When an appropriate screening for latent infections is not available, a tropical/infectious diseases specialist advice should be sought to evaluate the risk-benefit ratio of starting an immunomodulatory treatment and to set up a suitable clinical monitoring. F. In migrant patients with IA, vaccination should be performed according to the national recommendations of the country where the patient should be treated. Vaccination should be completed before starting biological treatment. G. In patients with IA, who have already started a biologic treatment, the risk of infection reactivation should be considered by a tropical/infectious diseases specialist according to the country specific potential exposure

Disease specific recommendations Agreement (SD)

Recommendation 1. Hansen’s disease (leprosy) should be ruled out in patients coming from high prevalence countries and presenting 9.69 (0.48)) unexplained cutaneous lesions or signs of peripheral neuropathy; biopsies of any suspicious skin lesion should be performed before starting biological treatment. Recommendation 2. NTM disease should be ruled out in patients with respiratory symptoms, evidence of bronchiectasis or other ar- 9.31 (1.14) chitectural lung abnormalities, regardless the country of origin. In these patients, smear and culture of three sputum specimens and/or bronchoalveolar lavage may be used to rule out NTM. Recommendation 3. Candidates to receive biological treatment coming from high prevalence countries for MDR-TB, and with positive 9.06 (0.93) LTBI screening, should be referred to a tropical/infectious specialist. Recommendation 4. Screening for brucellosis in asymptomatic patients is not recommended. Brucellosis should be ruled out in febrile 9.31 (1.01) patients coming from high prevalence countries and exposed to environmental risk factors (consumption of unpasteurised animal milk or direct contact with potentially infected animals). In these patients, serological and cultural tests should be performed before starting biological treatment. (grade of evidence II; strength of recommendation C; agreement (SD)) Recommendation 5. Salmonella spp. carrier status should be considered in patients coming from high prevalence countries, with 8.56 (1.36) cholelithiasis or defect in the urinary tract, in particular if previous episodes of fever and diarrhea are reported. However, stool or urine culture should be performed only on a case by case evaluation, before starting biological treatment. Recommendation 6. Screening for Leishmaniasis in asymptomatic patients is not recommended. Leishmaniasis should be ruled out 9.69 (0.60) in patients with fever, and/or hepatosplenomegaly and pancytopenia coming from endemic countries, before starting biological treatment. Recommendation 7. Babesiosis screening of asymptomatic patients coming from endemic countries is not recommended before start- 9.69 (0.60) ing biological treatment. Recommendation 8. Strongyloidiasis should be considered in all migrants from endemic areas and autochthonous patients with eo- 9.63 (0.72) sinophilia. In these patients, a serologic test, and when available a stool-based test, should be performed before starting biological treatment. Recommendation 9. Routinely screening of cysticercosis in asymptomatic patients before starting biological treatment is not recom- 9.69 (0.60)) mended. Neurocysticercosis should be ruled out in patients with epilepsy coming from endemic countries. Recommendation 10. Chagas disease should be considered in patients living or long-staying (>3 mo) in endemic areas, in patients 9.81 (0.40) whose mother was born in a Chagas disease endemic area and in patients who received a blood transfusion in endemic areas. In these patients serological testing should be performed before starting biological treatment. Recommendation 11. Chronic hepatitis E should be considered in patients with not otherwise explained liver enzymes abnormalities 9.44 (0.63) coming from countries with high prevalence. In these patients, serology should be performed before starting biological treatment. Recommendation 12. HTLV-1 screening of asymptomatic patients coming from endemic countries is not recommended before starting 9.56 (0.81) biological treatment. Recommendation 13. Histoplasmosis should be considered in patients coming from endemic areas. In these patients, a careful clinical 9.50 (0.52) history and chest radiography should be performed before starting biological treatment. In presence of suggestive history or radiological signs, serological and urinary antigen testing should be performed. Recommendation 14. Coccidioidomycosis should be considered in patients from endemic areas with a history of pneumonia, as- 9.19 (0.91) sociated to fatigue, arthralgias, and/or erythema nodosum. In these patients, serology should be performed before starting biological treatment. Recommendation 15. Paraccoccidioidomycosis should be ruled out in patients with not otherwise explained lung disease coming from 9.56 (0.63) areas with high prevalence. Screening of asymptomatic patients is not recommended before starting biological treatment.

5 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

Table IV. Disease-specific epidemiology: highly endemic areas of each pathogen.

Macroarea

Hansen’s disease Hansen’s Non tuberculous mycobacteria Multidrug resistant tuberculosis Brucellosis Salmonellosis Leishmaniasis Babesiosis Strongyloidiasis Cysticercosis Chagas disease HEV HTLV-1 Histoplasmosis Coccidioidomycosis Paraccoccidioidomycosis

Australia and New Zealand (Australia, New Zealand) Caribbean (Cuba, Dominican Republic, Haiti, Jamaica, Puerto Rico, X X The Bahamas, Trinidad and Tobago) Central America and Mexico (Belize, Costa Rica, El Salvador, Guatemala, X X X X X X X X X Honduras, Mexico, Nicaragua, Panama) Central Asia (Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, Uzbekistan) X X X X Eastern Africa (Burundi, Djibouti, Eritrea, Ethiopia, Kenya, Madagascar, X X X X X X X X X Malawi, Mozambique, Rwanda, Somalia, Somaliland, South Sudan, Uganda, United Republic of Tanzania, Zambia, Zimbabwe) Eastern Asia (China, Japan, Mongolia, North Korea, South Korea, Taiwan) X X X X X X Eastern Europe (Belarus, Bulgaria, Czech Republic, Hungary, Moldova, X Poland, Romania, Russia, Slovakia, Ukraine) Melanesia (Fiji, New Caledonia, Papua New Guinea, Solomon Islands, X X Vanuatu) Central Africa (Angola, Cameroon, Central African Republic, Chad, X X X X X X X Democratic Republic of the Congo, Equatorial Guinea, Gabon, Republic of Congo) Northern Africa (Algeria, Egypt, Libya, Morocco, Sudan, Tunisia, X X X X Western Sahara) Northern America (Canada, Greenland, USA) X X X X Northern Europe (Denmark, Estonia, Finland, Iceland, Ireland, Latvia, X Lithuania, Norway, Sweden, United Kingdom) Southern America (Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, X X X X X X X X X X X Falkland Islands, Guyana, Paraguay, Peru, Suriname, Uruguay, Venezuela) South-Eastern Asia (Brunei, Cambodia, East Timor, Indonesia, Laos, X X X X X X X Malaysia, Myanmar, Philippines, Thailand, Vietnam) Southern Africa (Botswana, Lesotho, Namibia, South Africa, Swaziland) X X X X X Southern Asia (Afghanistan, Bangladesh, Bhutan, India, Iran, Nepal, X X X X X X X Pakistan, Sri Lanka) Southern Europe (Albania, Bosnia and Herzegovina, Croatia, Greece, X Kosovo, Macedonia, Montenegro, Portugal, Republic of Serbia, Slovenia) Western Africa (Benin, Burkina Faso, Gambia, Ghana, Guinea, Guinea X X X X X X Bissau, Ivory Coast, Liberia, Mali, Mauritania, Niger, Nigeria, Senegal) Western Asia (Armenia, Azerbaijan, Cyprus, Georgia, Iraq, Israel, Jordan, Kuwait, Lebanon, Northern Cyprus, Oman, Palestine, Qatar, Saudi Arabia, X X X X Syria, Turkey, United Arab Emirates, Yemen) Western Europe (Austria, Belgium, France, Germany, Luxembourg, X Netherlands, Switzerland) monary extra-articular RA, overall co- architectural lung abnormalities, re- Multidrug resistant tuberculosis morbidities, asthma, COPD and GORD gardless the country of origin. In these (MDR-TB) than controls. patients, smear and culture of three MDR-TB is defined as a form of TB sputum specimens and/or bronchoal- resistant at least to isoniazid and ri- Recommendation 2 veolar lavage may be used to rule out fampicin, which requires longer, ex- NTM disease should be ruled out in NTM. (grade of evidence III; strength pensive and more toxic treatment regi- patients with respiratory symptoms, of recommendation D; agreement (SD) mens (45). MDR-TB cases have been evidence of bronchiectasis or other 9.31 (1.14)) reported in almost all countries, but the

6 Recommendations for infectious disease screening in migrants / F. Bartalesi et al. incidence in low resource countries is Recommendation 4 Recommendation 5 much higher and further increasing. No Screening for brucellosis in asymp- Salmonella spp. carrier status should be differences with latent TB have been tomatic patients is not recommended. considered in patients coming from high reported in patients with IA treated with Brucellosis should be ruled out in fe- prevalence countries, with cholelithiasis biologic. We suggest that patients com- brile patients coming from high preva- or defect in the urinary tract, in particu- ing from a high burden MDR-TB area, lence countries and exposed to environ- lar if previous episodes of fever and di- diagnosed with LTBI in the context of mental risk factors (consumption of un- arrhoea are reported. However, stool or a screening, other than MDR-TB con- pasteurised animal milk or direct con- urine culture should be performed only tact tracing, should receive LTBI treat- tact with potentially infected animals). on a case by case evaluation, before ment. This is suggested because, even In these patients, serological and cul- starting biological treatment. (grade of in those areas, the latent infections can tural tests should be performed before evidence III; strength of recommenda- be sustained by a susceptible strain of starting biological treatment. (grade of tion D; agreement (SD) 8.56 (1.36)) M. tuberculosis. evidence II; strength of recommendation C; agreement (SD) 9.31 (1.01)) Leishmaniasis Recommendation 3 Leishmaniasis is a protozoal zoonosis Candidates to receive biological treat- Salmonellosis caused by Leishmania spp, transmit- ment coming from high prevalence Typhoid fever is a severe systemic infected to humans by sand flies. The clini- countries for MDR-TB, and with posi- tion caused by the bacterium Salmonella cal spectrum includes cutaneous, mu- tive LTBI screening, should be referred enterica serotype typhi, characterized cocutaneous, and visceral (VL) forms. to a tropical/infectious disease special- by fever with or without accompanying The latter, classically characterised by ist. (grade of evidence IV; strength of symptoms (48). Other Salmonella sero- fever, hepatosplenomegaly and pancy- recommendation D; agreement (SD) types, particularly S. enterica serotype topenia, is fatal in 85-90% of cases if 9.06 (0.93)). paratyphi A, B, or C, can cause a simi- not treated (63). The leishmaniases are lar syndrome. Today, most of the burden widely dispersed, but most of the dis- Brucellosis of the disease occurs in countries where ease burden is concentrated in a few re- Brucellosis is one of the most com- sanitary conditions remain poor, with gions: close to 90% of VL cases occur mon and important zoonotic diseases a high incidence in South-central and in the Indian subcontinent, East Africa, worldwide. It is transmitted through the South-east Asia. The rest of Asia, Af- with the highest incidence in Ethiopia consumption of infected, unpasteurised rica, Latin America, the Caribbean, and and Sudan, and Brazil. Other foci are animal milk or direct contact with in- Oceania, except for Australia and New the Mediterranean Basin, the Middle fected wild and domestic animals. The Zealand, have a medium incidence (49). East and Central Asia, China and the human pathogens (Brucella abortus, Several cases of typhoid fever or other rest of South America. Several cases of B. suis, B. canis and B. melitensis) can diseases caused by Salmonella spp. have visceral leishmaniasis have also been cause systemic infections. The disease been reported in IA patients treated with reported in association with biolog- is widespread in European Mediterra- biologics, especially with anti-TNF. ics (11, 64-80), most of which were in nean countries, north and east Africa, Most infections were caused by S. en- Spain, one was also reported in Brazil, Middle East, south and central Asia and terica, in 14 cases. Few cases have been Portugal and France, however the pa- Central and South America. Only few reported for other serotypes, as paraty- tient was Algerian. Both visceral and cases of brucellosis have been reported phi in one case treated with infliximab, cutaneous cases of leishmaniasis have in association with anti-TNF-α treat- 1 case in S. dublin and S. enterica had- been reported in patients undergoing ment, two cases have been reported in dar. Few cases of septic arthritis caused anti-TNF monoclonal antibodies, but association with infliximab (46, 47). by Salmonella have been reported, one a relative-risk has not been definitely One infection was linked to consump- in association with etanercept. Based on established. Currently, there is no evi- tion of unpasteurised milk products. the Spanish register BIOBADASER, 17 dence supporting the screening in pa- Treatment was discontinued and an- cases of non-typhi Salmonella infections tients candidates to immunosuppres- timicrobial therapy was started with in patients with IA on anti-TNF therapy sants (81). resolution of the disease. were reported, of which 9 presented a At the time, there is no evidence sup- severe systemic infection, accounting Recommendation 6 porting a screening of patients who are for an incidence of 0.73/1000 PYs, with Screening for Leishmaniasis in asymp- to be treated with biologics, while bru- a relative risk (RR) of 2.07 (95% CI: tomatic patients is not recommended. cellosis should be considered in case 0.27–15.73), compared to IA patients not Leishmaniasis should be ruled out in of compatible symptoms/history, espe- receiving anti-TNF (14, 22, 31, 50-61). patients with fever, and/or hepatosple- cially if the patient comes from coun- General advice on measures to prevent nomegaly and pancytopenia coming tries with high prevalence. Finally, the faecal-oral transmitted diseases and to from endemic countries, before start- patients should be advised in order to avoid high-risk food reduces the risk of ing biological treatment. (grade of evi- avoid the consumption of unpasteurised Salmonella infections in RA patients dence III; strength of recommendation milk and cheese. receiving anti-TNF (62). D; agreement (SD) 9.69 (0.60))

7 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

Babesiosis test, should be performed before start- immigration from Latin America in the Tick-transmitted hemoparasites of the ing biological treatment. (grade of evi- last decade (91). protozoan genus Babesia are the second dence III; strength of recommendation There are only two reported cases of most common blood-borne parasites of D; agreement (SD) 9.63 (0.72)) RA and Chagas disease and neither of mammals after trypanosomes. Humans the patients was on biologic therapy are commonly infected by the bite of Cysticercosis (92, 93). Although the role of biologic an infected Ixodes tick. B. microti and Taenia solium is a cestode widely dif- drugs on Chagas disease progression is B. divergens are the two strains respon- fused in areas of poor hygienic condi- still unknown, screening for Chagas dis- sible for human disease in the United tions, characterised by improper dispos- ease should be performed in all patients States and Europe, respectively (82- al of human and pig feces (89). T. solium living or long-staying (>3 mo) in an en- 85). Occasionally, human babesiosis infection is endemic in less developed demic area, in patients whose mother has been reported from Australia, Tai- countries, in highlands or tropical areas, was born in a Chagas disease endemic wan, Japan and Korea (85, 86). in Central and South America, and non- area and in patients who received a Currently, there are no reports of babe- Muslim populations of South and South- blood transfusion in endemic areas. siosis in patients on biologics, and we East Asia and sub-Saharan Africa. The consider that, at the moment, a screen- accidental ingestion of its eggs can Recommendation 10 ing is not recommended. On the other cause cysticercosis (CC), characterised Chagas disease should be consid- hand, babesiosis should be considered by tissue invasion by the metacestode ered in patients living or long-staying in the differential diagnosis of febrile larval stage, occurring more frequently (>3 mo) in endemic areas, in patients illnesses in patients who report a tick in the central nervous system (neuro- whose mother was born in a Chagas bite from an endemic area. cysticercosis, NCC) (90). The symp- disease endemic area and in patients toms are related to the localisation of the who received a blood transfusion in en- Recommendation 7 cysts, their number and to the response demic areas. In these patients serologi- Babesiosis screening of asymptomatic of the host’s immune system (89). It is cal testing should be performed before patients coming from endemic coun- estimated that NCC causes about 30% starting biological treatment. (grade tries is not recommended before start- of cases of epilepsy in endemic, low re- of evidence III; strength of recommen- ing biological treatment. (grade of evi- sources countries (90). dation D; agreement (SD) 9.81 (0.40)) dence III; strength of recommendation No cases of cysticercosis have been D; agreement (SD) 9.69 (0.60)) reported in association with biologic HEV treatment. Currently, the screening it is Hepatitis E is an enterically-transmit- Strongyloidiasis not recommended in asymptomatic pa- ted, acute viral hepatitis. Hepatitis E Strongyloides stercoralis is a nematode tients. Epilepsy in adults coming from virus (HEV) is a RNA virus spread by which infects humans by direct penetra- endemic countries should be carefully faecal contaminated water and con- tion of skin in contact with contaminat- evaluated with a combination of crite- sumption of animal products in endem- ed soil. Walking barefoot is the main ria, including imaging data and sero- ic areas. Person-to-person transmission risk factor for the acquisition of the logical tests (89). is uncommon. Nosocomial and verti- infection, in areas with poor sanitary cal transmission, as well as via blood standards. It is endemic in tropical and Recommendation 9 transfusion, have also been described subtropical areas of the world including Routinely screening of cysticercosis (94). The highest incidence of HEV Southeast Asia, Latin America, sub- in asymptomatic patients before start- infection is in Asia, Africa, Middle Saharian Africa, and parts of the south- ing biological treatment is not recom- East and Central America. Most cases eastern US, but also in some temperate mended. Neurocysticercosis should be in western countries occur in travellers areas with low endemicity (87). So far, ruled out in patients with epilepsy com- returning from endemic areas, but spo- only one case of severe strongyloidiasis ing from endemic countries. (grade of radic cases not associated with travel has been reported in a Filipino patient evidence IV; strength of recommenda- have been reported, too (95). treated with adalimumab fo rRA (88). tion D; agreement (SD) 9.69 (0.60)) A recent retrospective study reported 23 All migrants from endemic areas and cases of HEV reactivation or infection autochthonous patients with eosino- Chagas disease in IA patients treated with biologics, philia should be screened before start- Chagas disease, also known as Ameri- mainly anti-TNF but also rituximab, ing any immunosuppressant therapy. can trypanosomiasis, is a neglected abatacept and tocilizumab (96-98). One parasitic infection caused by Trypano- case was also reported in the Orencia Recommendation 8 soma cruzi, endemic in South, Central and Rheumatoid Arhtritis (ORA) reg- Strongyloidiasis should be considered and part of North America (Mexico istry, the patient had been previously in all migrants from endemic areas and and possibly South Texas). Although treated with leflunomide and 3 differ- autochthonous patients with eosino- the vector is not present in Europe, the ent anti-TNF (etanercept, adalimumab philia. In these patients, a serologic disease has recently emerged in most and infliximab) and was concomitantly test, and when available a stool-based European countries, due to increasing treated with methotrexate 15 mg/week

8 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

(99). Few infections were linked to re- developed ATL. However, HTLV-1– case reports and small case series, the cent travels to Spain and consumption positive patients with RA had higher recommendations regarding diagnosis of contaminated chorizo, while one inflammation and greater resistance to and management are based on expert case with uncooked shellfish. anti-TNF treatment than HTLV-1–neg- opinion (128, 129). However, in pa- The screening for HEV is not recom- ative patients (105). tients coming from endemic areas, a mended routinely, but the use of di- At the moment, there is no evidence screening for a clinical history of his- agnostic test (serologic and molecular supporting the indication of HTLV-1 toplasmosis and a chest radiography test) before and during treatment with screening in IA patients from endemic should be considered. In presence of biologics should be considered in mi- areas, candidates to biological treat- a history of pulmonary infection, and/ grants with unexplained liver enzymes ment. or of radiographic findings showing in- abnormalities. Finally, travellers to filtrates, nodules, or lymphadenopathy endemic areas should be advised to Recommendation 12 without a clear etiology, serology for prevent faecal-orally transmitted infec- HTLV-1 screening of asymptomatic pa- Histoplasma should be performed. tions, such as avoiding drinking water tients coming from endemic countries of unknown purity, uncooked shellfish, is not recommended before starting bi- Recommendation 13 and uncooked fruits or vegetables. ological treatment. (grade of evidence Histoplasmosis should be considered III; strength of recommendation D; in patients coming from endemic areas. Recommendation 11 agreement (SD) 9.56 (0.81)) In these patients, a careful clinical his- Chronic hepatitis E should be con- tory and chest radiography should be sidered in patients with not otherwise Histoplasmosis performed before starting biological explained liver enzymes abnormali- Histoplasma capsulatum is a dimorphic treatment. In presence of suggestive ties coming from countries with high fungus responsible for the most com- history or radiological signs, serologi- prevalence. In these patients, serology mon endemic mycosis causing human cal and urinary antigen testing should should be performed before starting bi- infection. The endemic area includes be performed. (grade of evidence III; ological treatment. (grade of evidence the Ohio and Mississippi River val- strength of recommendation D; agree- III; strength of recommendation D; leys, Central and South America, and ment (SD) 9.50 (0.52)) agreement (SD) 9.44 (0.63)) microfoci in the Eastern United States, southern Europe, Africa, and South- Coccidioidomycosis Human T-lymphotropic virus eastern Asia (106). In immunocompe- Coccidioidomycosis is caused by in- (HTLV-I) tent individuals, the infection is usually halation of spores (arthroconidia) of This is a RNA human retrovirus, esti- a self-limited febrile illness although dimorphic fungi of the genus Coc- mated to infect 10 to 20 million peo- occasionally it evolves toward a chron- cidioides. These are endemic in some ple worldwide, but is associated with ic pulmonary infection. Conversely, deserts in the United States (Arizona, disease in less than 5% of infected in- immunosuppression and immunosup- California, New Mexico and Texas), in dividuals. HTLV-1 is transmitted by pressants, including biologic and other parts of Mexico and Central and South breast feeding, although transmission immunomodulatory therapies for rheu- America (130). also can occur via blood transfusion, matic diseases, are a well-known risk Several cases of coccidioidomycosis sexual intercourse or sharing of needles. factor for life-threatening disseminated have been reported in IA patients receiv- In some areas in Japan, sub-Saharan Af- forms, extrapulmonary disease or reac- ing biologics (14, 20, 31, 131-136). The rica, the Caribbean and South America tivation of latent infections (107, 108). infections were localised, mainly pneu- more than 1% of the general population Histoplasmosis might be the most com- monia, or disseminated, while few cases is infected (100, 101). The virus is as- mon invasive fungal infection reported were asymptomatic and diagnosed after sociated with three categories of severe in patient receving biologic agents, and testing. Most of the patients were from disease: hematologic malignancy (adult several cases of histoplasmosis have Arizona, Texas, New Mexico. T-cell leukaemia/lymphoma) (ATL), in- been widely reported (14, 31, 59, 107, Based on these observations, in pa- flammatory syndromes (HTLV-1-asso- 109-127). Nine cases of histoplasmo- tients coming from US States of Ari- ciated myelopathy/tropical spastic para- sis have been reported in the SABER zona, California, New Mexico and paresis, arthropathy and uveitis among (Safety Assessment of Biologic Thera- Texas or from endemic areas of Mex- others), and opportunistic infections py) Study, conducted in the USA (14). ico, Central and South America, an ac- (including Strongyloides stercoralis Most patients developed pulmonary curate clinical history should be taken hyperinfection and others) (101-103). histoplasmosis, but progressive dissem- to detect a possible, previous symp- HTLV-1-associated arthropathy resem- ination, and also panniculitis and focal tomatic coccidioidomycosis and coc- bles RA, with synovial proliferation and myositis have been described. Fatal cidioidal serology prior to biological a positive rheumatoid factor (104). cases may also occur. therapy should be considered. Specific Ten HTLV-1–positive patients with Since most of the available clinical in- serologic tests (immunodiffusion, tube RA have been treated with anti-TNF, formation on histoplasmosis in patients precipitin-reacting antigen, comple- and during 2 years of observation none receiving anti-TNF agents is based on ment fixation, enzyme-linked immuno-

9 Recommendations for infectious disease screening in migrants / F. Bartalesi et al. assay) for both IgM and IgG antibodies a new wave that has raised the concern published recommendations for the are available. Direct smear examina- at EU and international level. Unfor- diagnosis and management of intesti- tion and sputum culture can be useful tunately, high-grade evidence on the nal parasitic infections in patients with in course of pneumonia. risk of reactivation of latent infections rheumatic diseases, (RA, systemic lu- in this population, and on the utility of pus erythematosus and spondyloarthri- Recommendation 14 screening and prophylaxis strategies tis) (140). Coccidioidomycosis should be consid- is not available. The highest grade of Moreover, it is important to stress the ered in patients from endemic areas strength of a recommendation is there- fact that migrants and travellers, af- with a history of pneumonia, associated fore C. The literature on diagnostic ac- fected by rheumatic diseases, may have to fatigue, arthralgias, and/or erythema curacy of screening tests as well as on travelled in several countries before nodosum. In these patients, serology the efficacy of prophylaxis in the gener- getting to the European soil. Therefore, should be performed before starting bi- al population without IA were not sys- the rheumatologist should always ob- ological treatment. (grade of evidence tematically reviewed, and the experts tain detailed information on the coun- III; strength of recommendation D; formulated recommendations based on tries visited to create the map of the risk agreement (SD) 9.19 (0.91)) their knowledge and experience. A pre- and orientate the investigation for an liminary search on the migratory flows occult infectious/parasitic diseases, Paraccoccidioidomycosis and country-specific relative risks of .For preventive measures, no sufficient Paracoccidioidomycosis is an inflam- latent, hidden or opportunistic infection data were available to draw conclusions matory granulomatous systemic disease was performed, although not system- in the specific sub-population of mi- endemic in Latin America from Mexico atically, in order to define the potential grant people. Therefore, for these rec- to Argentina due to a dimorphic fungus, burden of such infections. Our litera- ommendations the experts have taken Paracoccidioides brasiliensis (137). In ture search focused essentially on three into account their knowledge of and recent years, a rise in imported paracoc- important aspects of migration-related experience on the general population. cidioidomycosis has been observed in infectious risk: the incidence of latent Regarding the vaccination policies to Europe, due to the increase of interna- and opportunistic infections in IA on be applied to IA population, consider- tional travels and migrant flows (138). biologics, the potentially advantage of ing the indication, the efficacy and the So far, one case of paracoccidioidomy- a screening and the efficacy and safety safety of each vaccination, the panel cosis associated with biologic therapies of prophylaxis measures. agreed on considering the need of a spe- has been reported in patient living in We should acknowledge that the grad- cific document to address this complex Brazil (139). ing of the available evidence can dif- issue. At the moment, the panel agreed Currently we consider that an active fer between the three aforementioned that in migrant IA patients vaccinations screening of the disease is not recom- aspects: higher level evidence is avail- should be performed according to the mended. able for the incidence of infections in national recommendations of the coun- IA patients on biologics, but with little try where the patient is treated with bio- Recommendation 15 information (even absent) on the origin logic agents. Paraccoccidioidomycosis should be of patients, and most studies are under- The results of agreement voting are ruled out in patients with not otherwise powered with regard to rare exposure. therefore of particular importance since explained lung disease coming from Not even the new registers that have they represent the overall interpretation areas with high prevalence. Screen- been established in developing coun- by the panel of experts of the evidence ing of asymptomatic patients is not tries (South Africa, Brazil) have yet on all aforementioned aspects of infec- recommended before starting biologi- provided information about the risk of tious risk in migrant patients with IA cal treatment. (grade of evidence III; infection in settings with high exposure starting biologics, in particular looking strength of recommendation D; agree- to infectious agents relevant to migrant at the new biological drugs available in ment (SD) 9.56 (0.63)) populations. In particular, helminths 2016 (141). and protozoa that are parasites of the The recommendations will need to be Discussion gastrointestinal tract are most preva- updated on a regular basis, since epide- These recommendations for infectious lent in tropical regions. For this reason, miological changes will occur over the disease screening in migrant patients patients and travellers derived from time and new evidence hopefully will with IA starting biologic drugs are these areas with a diagnosis of a rheu- become available with regard to current based on the current evidence resulting matic disease may be at high risk for a and new biologic drugs and emerging from the systematic literature review significant re-exacerbation of the in- infectious risks. and the opinion of selected experts in testinal disease. Therefore, the rheuma- Other infections might be added to this the fields of rheumatology and tropi- tologist should always be very vigilant list in the future, considering that the cal/infectious diseases from Italy and when migrants or travellers affected possible increase of immunosuppres- Spain. These two countries have expe- with rheumatic diseases derive from sant therapies in low-income countries rienced a significant flow of migrants in these continents. In fact, the Brazilian might permit to identify other agents the last decade and are currently facing Society of Rheumatology has already with the same characteristics.

10 Recommendations for infectious disease screening in migrants / F. Bartalesi et al.

Key messages following etanercept treatment for arthritis. activity and remission with adalimumab plus • Few data are available on the risk of Clin Rheumatol 2012; 31: 395-8. methotrexate or methotrexate alone in early 11. KHAN A, COAKLEY G, COSGROVE C, LOCK- rheumatoid arthritis: 26-week results from latent infections reactivation in mi- WOOD D: Let off the leash: kala-azar fol- the randomised, controlled OPTIMA study. grants lowing the use of tumour necrosis factor Ann Rheum Dis 2013; 72: 64-71. • The individual risk of infectious antibodies. BMJ Case Rep 2010 (2010). 25. KLUGER N, COHEN P, FALLET-BIANCO C, diseases should be estimated on the 12. BURMESTER GR, RUBBERT-ROTH A, CAN- GUILLEVIN L: Mycobacterium chelonae in- TAGREL A et al.: Efficacy and safety of sub- fection under adalimumab therapy for spon- basis of epidemiological risk in the cutaneous tocilizumab versus intravenous dylarthritis. Clin Exp Rheumatol 2010; 28: country of origin tocilizumab in combination with traditional 101-2. • When an infectious disease is sus- DMARDs in patients with RA at week 97 26. KOBAYASHI D, ITO S, HIRATA A et al.: (SUMMACTA). Ann Rheum Dis 2016; 75: Mycobacterium abscessus pulmonary infec- pected, appropriate screening should 68-74. tion under treatment with tocilizumab. In- be performed 13. HOEFSLOOT W, van INGEN J, ANDREJAK C tern Med (Tokyo, Japan) 2015; 54: 1309-13. • Tropical/infectious disease special- et al.: Mycobacteria Network European Tri- 27. KOIKE T, HARIGAI M, INOKUMA S et al.: ist advice should be sought when als, The geographic diversity of nontubercu- Postmarketing surveillance of tocilizumab lous mycobacteria isolated from pulmonary for rheumatoid arthritis in Japan: interim screening for latent infections is not samples: an NTM-NET collaborative study. analysis of 3881 patients. Ann Rheum Dis available Eur Respir J 2013; 42: 1604-13. 2011; 70: 2148-51. 14. BADDLEY JW, WINTHROP KL, CHEN L et 28. KOIKE T, HARIGAI M, ISHIGURO N et al.: Acknowledgements al.: Non-viral opportunistic infections in Safety and effectiveness of adalimumab in new users of tumour necrosis factor inhibi- Japanese rheumatoid arthritis patients: post- The authors wish to acknowledge the tor therapy: results of the SAfety Assess- marketing surveillance report of the first support of the Italian Society for Rheu- ment of Biologic ThERapy (SABER) study. 3,000 patients. Mod Rheumatol 2012; 22: matology Ann Rheum Dis 2014; 73: 1942-8. 498-508. 15. BAKKER CV, KARDAUN SH, WILTING KR, 29. KOMANO Y, TANAKA M, NANKI T et al.: In- DIERCKS GF, HORVATH B: Why you should cidence and risk factors for serious infection References ask your patients about their fishing hob- in patients with rheumatoid arthritis treated 1. FURST DE: The risk of infections with bio- bies. 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MARIETTE X, BERTIN P, ARENDT C, TERP- sues in a globalized world: threats, risks and 2002; 8: 265-8. STRA I, VanLUNEN B, De LONGUEVILLE M: challenges, an evidence-based framework. 18. COLLINS CS, TERRELL C, MUELLER P: Dis- Pooled analysis of the risk of serious infec- Emerg Health Threats J 2009; 2: e10. seminated Mycobacterium haemophilum tions and opportunistic infections in clinical 4. BARTALESI F, BARTOLONIA, BISOFFI Z et infection in a 72-year-old patient with rheu- trials of certolizumab pegol for rheumatoid al.: The emerging problem of biological matoid arthritis on infliximab. BMJ Case arthritis. Rheumatology (United Kingdom) treatment in migrant and travelling popula- Rep 2013; 2013. 2012; 51: iii132. tions: it is time to extend guidelines for the 19. DANKO JR, GILLILAND WR, MILLER RS, 32. MIN Z, AMLANI M: Pulmonary Mycobacte- screening of infectious diseases. Ann Rheum DECKER CF: Disseminated Mycobacterium rium kansasii Infection Mimicking Malig- Dis 2014; 73: 794-6. marinum infection in a patient with rheuma- nancy on the (18)F-FDG PET Scan in a Pa- 5. van der HEIJDE D, ALETAHA D, CARMONA toid arthritis receiving infliximab therapy. tient Receiving Etanercept: A Case Report L et al.: 2014 Update of the EULAR stand- Scand J Infect Dis 2009; 41: 252-5. and Literature Review. Case Rep Pulmonol ardised operating procedures for EULAR- 20. GENOVESE MC, RUBBERT-ROTH A, SMOLEN 2014; 2014: 973573. endorsed recommendations. Ann Rheum Dis JS et al.: Longterm safety and efficacy of to- 33. NAKAHARA H, KAMIDE Y, HAMANO Y et 2015; 74: 8-13. cilizumab in patients with rheumatoid arthri- al.: A case report of a patient with rheuma- 6. WHO Expert Committee on Leprosy, World tis: a cumulative analysis of up to 4.6 years of toid arthritis complicated with Mycobacte- Health Organization technical report series exposure. 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