Mycobacteriosis in Pigs – An Underrated Threat

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Although Mycobacterium avium subspecies are generally not considered food pathogens, the infections caused by these particular nontuberculous mycobacteria (NTM) can represent a serious threat to immunocompromised population. Additionally, infections with a member of Mycobacterium Avium Compex (MAC) can affect the efficiency of BCG vaccines used for the humans. In infected animals, M. avium may be present in different tissues without apparent clinical symptoms and macroscopic lesions. Veterinary meat inspection would then fail to recognize infected animals and such meat and meat products thereof could enter the human diet. The aim of this paper is also to analyze the current control policy in Europe according to infections of pigs with the members of MAC, and point out the risks for public health. By analyzing a large number of meat samples and other dietary nutrients, different groups of authors have provided evidence to support the hypothesis that M. avium is present in the everyday environment. Therefore, food as a source of infection with mycobacteria should not be ignored. The control of mycobacteria requires a better diagnostic approach, having in mind recent positive cases of M. avium subspecies hominissuis (MAH) in an increasing number of exported pigs from EU countries to Serbia. The introduction of reliable diagnostic methods for MAH could result in decreasing the occurrence of infection in pigs, as well as in humans, having in mind that WHO reported 10 million new cases of tuberculosis-mycobacteriosis in the human population in 2015 with 21% of these cases occurring in immunocompromised individuals and children.


  • 1. Falkinham JO. Surrounded by mycobacteria: Nontuberculous mycobacteria in the human environment. J Appl Microbiol. 2009;107(2):356-67.

  • 2. Falkinham JO. Nontuberculous Mycobacteria: Community and Nosocomial Waterborne Opportunistic Pathogens. Clin Microbiol Newsl. 2016;38(1):1-7.

  • 3. Rindi L, Buzzigoli A, Medici C, Garzelli C. High phylogenetic proximity of isolates of Mycobacterium avium subsp. hominissuis over a two decades-period. Infect Genet Evol. 2013;16:99-102.

  • 4. Klanicova-Zalewska B, Slana I. Presence and persistence of Mycobacterium avium and other nontuberculous mycobacteria in animal tissues and derived foods: A review. Meat Sci. 2014;98(4):835-41.

  • 5. Dziedzinska R, Makovcova J, Kaevska M, Slany M, Babak V, Moravkova M. Nontuberculous Mycobacteria on Ready-to-Eat, Raw and Frozen Fruits and Vegetables. J Food Prot. 2016;79(8):1452-6.

  • 6. Kriz P, Kaevska M, Slana I, Bartejsova I, Pavlik I. Mycobacterium avium subsp. avium in lymph nodes and diaphragms of pigs from one infected herd in the czech republic. J Food Prot. 2014;77(1):141-4.

  • 7. Slana I, Kaevska M, Kralik P, Horvathova A, Pavlik I. Distribution of Mycobacterium avium subsp. avium and M. a. hominissuis in artificially infected pigs studied by culture and IS901 and IS1245 quantitative real time PCR. Vet Microbiol. 2010;144(3-4):437-43.

  • 8. Polaček V, Becskei Z, Vidanović D, Prodanov-Radulović J, Aleksić-Kovačević S. Detection of Mycobacterium avium subsp. hominissuis in lymph nodes with and without gross lesions from tuberculin skin test-positive pigs. J Comp Pathol. 2015 Jan;152(1):83.

  • 9. Kolb J, Hillemann D, Möbius P, Reetz J, Lahiri A, Lewin A, Rüsch-Gerdes S, Richter E. Genetic characterization of German Mycobacterium avium strains isolated from different hosts and specimens by multilocus sequence typing. Int J Med Microbiol. 2014;304(8):941-8.

  • 10. Schinköthe J, Möbius P, Köhler H, Liebler-Tenorio EM. Experimental Infection of Goats with Mycobacterium avium subsp. hominissuis: A Model for Comparative Tuberculosis Research. J Comp Pathol. 2015;155(2-3):218-30.

  • 11. Kim M-C, Kim J, Kang W, Jang Y, Kim Y. Systemic infection of Mycobacterium avium subspecies hominissuis and fungus in a pet dog. J Vet Med Sci. 2015;78(1):1-4.

  • 12. Beck A, Špičić S, Butorović-Dujmović M, Račić I, Huber D, Kurilj AG, Beck R, Cvetnić. Mucocutaneous Infl ammatory Pseudotumours in Simultaneous Mycobacterium avium subsp. avium and Mycobacterium avium subsp. hominissuis Infection in a Cat. J Comp Pathol. 2015 Nov;153(4):227-30.

  • 13. Pate M, Zajc U, Kušar D, Žele D, Vengušt G, Pirš T, Ocepek M. Mycobacterium spp. in wild game in Slovenia. Vet J. 2016;208:93-5.

  • 14. Barthel Y, Drews S, Fehr M, Moser I, Matz-Rensing K, Baumgartner W, Wohlsein P. Concurrent infection with Mycobacterium avium subsp. hominissuis and Giardia duodenalis in a chinchilla (Chinchilla lanigera f. dom.). Berl Munch Tierarztl Wochenschr. 2016;129(5-6):242-6.

  • 15. Kriz P, Jahn P, Bezdekova B, Blahutkova M, Mrlik V, Slana I, Pavlik I. Mycobacterium avium subsp. hominissuis infection in horses. Emerg Infect Dis. 2010;16(8):1328-9.

  • 16. Dagleish MP, Stevenson K, Foster G, McLuckie J, Sellar M, Harley J, Evans J, Brownlow A. Mycobacterium avium subsp. hominissuis Infection in a Captive-Bred Kiang (Equus kiang). J Comp Pathol. 2012;146(4):372-7.

  • 17. Arrazuria R, Sevilla IA, Molina E, Pérez V, Garrido JM, Juste RA, Elguezabal N. Detection of Mycobacterium avium subspecies in the gut associated lymphoid tissue of slaughtered rabbits. BMC Vet Res. 2015;11(1):130.

  • 18. Moravkova M, Mrlik V, Parmova I, Kriz P, Pavlik I. High incidence of Mycobacterium avium subspecies hominissuis infection in a zoo population of bongo antelopes (Tragelaphus eurycerus). J Vet Diagn Invest. 2013;25(4):531-4.

  • 19. Bezos J, Álvarez-Carrión B, Rodríguez-Bertos A, Fernández-Manzano Á, de Juan L, Huguet C, Briones V, Romero B. Evidence of disseminated infection by Mycobacterium avium subspecies hominissuis in a pet ferret (Mustela putorius furo). Vol. 109, Research in Veterinary Science. 2016.

  • 20. Lahiri A, Kneisel J, Kloster I, Kamal E, Lewin A. Abundance of Mycobacterium avium ssp. hominissuis in soil and dust in Germany - implications for the infection route. Lett Appl Microbiol. 2014;59(1):65-70.

  • 21. Vaerewijck MJM, Huys G, Palomino JC, Swings J, Portaels F. Mycobacteria in drinking water distribution systems: ecology and significance for human health. FEMS Microbiol Rev. 2005;29(5):911-34.

  • 22. Matlova L, Dvorska L, Ayele WY, Bartos M, Amemori T, Pavlik I. Distribution of Mycobacterium avium complex isolates in tissue samples of pigs fed peat naturally contaminated with mycobacteria as a supplement. J Clin Microbiol. 2005;43(3):1261-8.

  • 23. Matlova L, Dvorska L, Palecek K, Maurenc L, Bartos M, Pavlik I. Impact of sawdust and wood shavings in bedding on pig tuberculous lesions in lymph nodes, and IS1245 RFLP analysis of Mycobacterium avium subsp. hominissuis of serotypes 6 and 8 isolated from pigs and environment. Vet Microbiol. 2004;102(3-4):227-36.

  • 24. Fischer O A, Matlova L, Dvorska L, Svastova P, Peral DL, Weston RT, Bartos M, Pavlik I. Beetles as possible vectors of infections caused by Mycobacterium avium species. Vet Microbiol. 2004;102(3-4):247-55.

  • 25. Fischer OA, Matlova L, Dvorska L, Svastova P, Bartl J, Weston RT, Pavlik I. Blowfl ies Calliphora vicina and Lucilia sericata as passive vectors of Mycobacterium avium subsp. avium, M.a. paratuberculosis and M.a. horminissuis. Med Vet Entomol. 2004;18(2):116-22.

  • 26. Johansen TB, Agdestein A, Lium B, Jørgensen A, Djønne B. Mycobacterium avium subsp. hominissuis infection in swine associated with peat used for bedding. Biomed Res Int. 2014;2014:189649.

  • 27. Agdestein A, Olsen I, Jørgensen A, Djønne B, Johansen TB. Novel insights into transmission routes of Mycobacterium avium in pigs and possible implications for human health. Vet Res. 2014;45:46.

  • 28. Johansen T, Agdestein A, Olsen I, Nilsen S, Holstad G, Djønne B, Turenne C. Biofi lm formation by Mycobacterium avium isolates originating from humans, swine and birds. BMC Microbiol. 2009;9(1):159.

  • 29. Milanov D, Prunić B, Velhner M, Todorović D, Polaček V. Investigation of biofi lm formation and phylogenetic typing of Escherichia coli strains isolated from milk of cows with mastitis. Acta Vet Belgrade. 2015;65(2):202-16.

  • 30. Čabarkapa I, Škrinjar M, Lević J, Kokić B, Blagojev N, Milanov D, Suvajdžić L. Biofilm forming ability of Salmonella enteritidis in vitro. Acta Vet Belgrade. 2015;65(3):371-89.

  • 31. Faria S, Joao I, Jordao L. General Overview on Nontuberculous Mycobacteria, Biofilms, and Human Infection. J Pathog. 2015;2015:1-10.

  • 32. Johansen TB. Characterisation of Isolates of Mycobacterium avium with emphasis on IS elements and biofilm abilities. The Norwegian School of Veterinary Science; 2009.

  • 33. Rindi L, Garzelli C. Genetic diversity and phylogeny of Mycobacterium avium. Infect Genet Evol. 2014;21:375-83.

  • 34. Inderlied CB, Kemper CA, Bermudez LE. The Mycobacterium avium complex. Clin Microbiol Rev. 1993;6(3):266-310.

  • 35. Falkinham JO. Epidemiology of infection by nontuberculous mycobacteria . Epidemiology of Infection by Nontuberculous Mycobacteria. Clin Microbiol Rev. 1996;9(2):177-215.

  • 36. Karakousis PC, Moore RD, Chaisson RE. Mycobacterium avium complex in patients with HIV infection in the era of highly active antiretroviral therapy. Lancet Infect Dis. 2004;4(9):557-65.

  • 37. Bull TJ, Mcminn EJ, Sidi-boumedine K, Skull A, Durkin D, Neild P, Rhodes G, Pickup R, Hermon-taylor J. Detection and Verification of Mycobacterium avium subsp . paratuberculosis in Fresh Ileocolonic Mucosal Biopsy Specimens from Individuals with and without Crohn’ s Disease Detection and Verifi cation of Mycobacterium avium subsp. paratuberculosis in Fres. J Clin Microbiol. 2003;41(7):2915-23.

  • 38. Grant IR. Zoonotic potential of Mycobacterium avium ssp. paratuberculosis: The current position. J Appl Microbiol. 2005;98(6):1282-93.

  • 39. Rodrick J. Chiodini, William M. Chamberlin, Jerzy Sarosiek RWM. Crohn’s disease and the mycobacterioses: A quarter century later. Causation or simple association? Crit Rev Microbiol. 2012;38(1):52-93.

  • 40. Weller R, Skrypnyk A, Zavgorodniy A, Stegniy B, Gerilovych A, Kutsan O, Pozmogova S, Sapko S. The bovine tuberculosis burden in cattle herds in zones with low dose radiation pollution in Ukraine. Vet Ital. 2009;45(2):225-33.

  • 41. Cossu D, Masala S, Frau J, Cocco E, Marrosu MG, Sechi LA. Anti Mycobacterium avium subsp. paratuberculosis heat shock protein 70 antibodies in the sera of Sardinian patients with multiple sclerosis. J Neurol Sci. 2013;335(1):131-3.

  • 42. Lara GHB, Ribeiro MG, Leite CQF, Paes AC, Guazzelli A, Silva AV da, Santos ACB, Listoni FJP. Occurrence of Mycobacterium spp. and other pathogens in lymph nodes of slaughtered swine and wild boars (Sus scrofa). Res Vet Sci. 2011;90(2):185-8.

  • 43. Dvorska L, Matlova L, Bartos M, Parmova I, Bartl J, Svastova P, Bull T., Pavlik I. Study of Mycobacterium avium complex strains isolated from cattle in the Czech Republic between 1996 and 2000. Vet Microbiol. 2004;99(3):239-50.

  • 44. Ichikawa K, van Ingen J, Koh WJ, Wagner D, Salfi nger M, Inagaki T, Uchiya K ichi, Nakagawa T, Ogawa K, Yamada K, Yagi T. Genetic diversity of clinical Mycobacterium avium subsp. hominissuis and Mycobacterium intracellulare isolates causing pulmonary diseases recovered from different geographical regions. Infect Genet Evol. 2015;36:250-5.

  • 45. Pate M, Žolnir-Dovč M, Krt B, Ocepek M. IS1245 RFLP-based genotyping study of Mycobacterium avium subsp. hominissuis isolates from pigs and humans. Comp Immunol Microbiol Infect Dis. 2008;31(6):537-50.

  • 46. Iwamoto T, Nakajima C, Nishiuchi Y, Kato T, Yoshida S, Nakanishi N, Tamaru A, Tamura Y, Suzuki Y, Nasu M. Genetic diversity of Mycobacterium avium subsp. hominissuis strains isolated from humans, pigs, and human living environment. Infect Genet Evol. 2012;12(4):846-52.

  • 47. Ogawa K, Ichikawa K, Hasegawa Y, Inagaki T, Yagi T, Nakagawa T, Moriyama M, Adachi T. Molecular typing and genetic characterization of Mycobacterium avium subspecies hominissuis isolates from humans and swine in Japan. J Med Microbiol. 2016;

  • 48. Starkova DA, Mokrousov IV, Viazovaia AA, Zhuravlev VI, Otten TF, Vishnevskiĭ BI, Narvskaia OV. The genome polymorphism of the Mycobacterium avium subsp. hominissuis strains. Mol Gen Mikrobiol Virusol. 2014;(4):14-9.

  • 49. Andersen P, Doherty TM. The success and failure of BCG-implication for a novel tuberculosis vaccine. Nat Rev Microbiol. 2005;3:657-62.

  • 50. Andersen P. Tuberculosis vaccine- an update. Nat Rev Microbiol. 2007;5:484-7.

  • 51. Graham R, Stewart BDR a. DBY. Tuberculosis: A Problem with Persistence. Nat Rev Microbiol. 2003;1:97-105.

  • 52. Campbell IA. Opportunist (environmental) mycobacterial diseases. Medicine (Baltimore). 2008;36(6):306-8.

  • 53. Agdestein A, Johansen TB, Polaček V, Lium B, Holstad G, Vidanović D, Aleksić-Kovačević S, Jørgensen A, Žultauskas J, Nilsen SF, Djønne B. Investigation of an outbreak of mycobacteriosis in pigs. BMC Vet Res. 2011;7:63.

  • 54. Polaček V, Prodanov-Radulović J, Vidanović D, Kovačević-Aleksić S. Comparision of Macroscopic and Microscopic Lession in Mesenterial Lymph Nodes In Pigs Naturally infected with Mycobacterium avium subsp hominissuis. In: Petrović T, editor. Book of Abstracts “One World New Challenges”-First International Symposium of Veterinary Medicine- ISVM2015, Vrdnik Serbia. Vrdnik,: Scientifi c Veterinary Institute Novi Sad, Novi Sad, Serbia; 2015. p. 42-9.

  • 55. Cvetnić Ž, Špičić S, Duvnjak S, Zdelar-Tuk M, Benić M, Mitak M, Pate M, Krt B, Ocepek M. High Prevalence of Mycobacterium avium subsp. hominissuis in a batch of quarantined pigs in Croatia. Slov Vet Res. 2009;46(4):149-54.

  • 56. Faldyna M, Göpfert E, Kudlackova H, Stepanova H, Kaevska M, Slana I, Pavlik I. Usability of a gamma interferon release assay in the diagnosis of naturally infected pigs with Mycobacterium avium subspecies hominissuis. J Vet Diagn Invest. 2012;24(2):376-8.

  • 57. Orme IM, Basaraba RJ. The formation of the granuloma in tuberculosis infection. Semin Immunol. 2014;26(6):601-9.

  • 58. Ulrichs T, Kaufmann SHE. New insights into the function of granulomas in human tuberculosis. J Pathol. 2006;208(2):261-9.

  • 59. Miranda C, Matos M, Pires I, Correia-Neves M, Ribeiro P, Álvares S, Vieira-Pinto M, Coelho AC. Diagnosis of Mycobacterium avium Complex in Granulomatous Lymphadenitis in Slaughtered Domestic Pigs. Vol. 147, Journal of Comparative Pathology. 2012.

  • 60. Domingos M, Amado a., Botelho a. IS1245 RFLP analysis of strains of Mycobacterium avium subspecies hominissuis isolated from pigs with tuberculosis lymphadenitis in Portugal. Vet Rec. 2009;164(4):116-20.

  • 61. Pate M, Zdovc I, Pirs T, Krt B, Ocepek M. Isolation and characterisation of Mycobacterium avium and Rhodococcus equi from granulomatous lesions of swine lymph nodes in Slovenia. Acta Vet Hung. 2004;52(2):143-50.

  • 62. Sakai M, Ohno R, Higuchi C, Sudo M, Suzuki K, Sato H, Maeda K, Sasaki Y, Kakuda T, Takai S. Isolation of Rhodococcus equi from wild boars (Sus scrofa) in Japan. J Wildl Dis. 2012; 48(3):815-7.

  • 63. Sevilla IA, Molina E, Elguezabal N, Pérez V, Garrido JM, Juste RA. Detection of mycobacteria, Mycobacterium avium subspecies, and Mycobacterium tuberculosis complex by a novel tetraplex real-time PCR assay. J Clin Microbiol. 2015;53(3):930-40.

  • 64. Polaček V. The role of myofi broblast in morphogenesis of granulomatous lymphadenitis in pigs naturally infected with Mycobacterium avium complex. Doctoral Dissertation, Faculty of Veterinary Medicine, University of Belgrade; 2010.

  • 65. Monaghan,M.L., Doherty, M.L., Collins, J.D., Kazda, J.F., Quinn PJ. The tuberculin test. Veterinary Microbiology. 1994;40:111-24.

  • 66. Ulrichs T, Lefmann M, Reich M, Morawietz L, Roth A, Brinkmann V, Kosmiadi GA, Seiler P, Aichele P, Hahn H, Krenn V, Göbel UB, Kaufmann SHE. Modifi ed immunohistological staining allows detection of Ziehl-Neelsen-negative Mycobacterium tuberculosis organisms and their precise localization in human tissue. J Pathol. 2005;205(5):633-40.

  • 67. K. Sakamoto. The Pathology of Mycobacterium tuberculosis Infection. Vet Pathol. 2012;49(3):423-39.

  • 68. Bradner LK. Optimization of methods for culturing Mycobacterium avium subsp. paratuberculosis from bovine milk and colostrum and application to samples collected from naturally infected dairy cows. 2013;

  • 69. Álvarez J, Castellanos E, Romero B, Aranaz a, Bezos J, Rodríguez S, Mateos a, Domínguez L, de Juan L. Epidemiological investigation of a Mycobacterium avium subsp. hominissuis outbreak in swine. Epidemiol Infect. 2011;139(1):143-8.

  • 70. Kaevska M, Slana I, Kralik P, Reischl U, Orosova J, Holcikova A, Pavlik I. “Mycobacterium avium subsp. hominissuis” in neck lymph nodes of children and their environment examined by culture and triplex quantitative real-time PCR. J Clin Microbiol. 2011;49(1):167-72.

  • 71. Slana I, Kaevska M, Kralik P, Horvathova A, Pavlik I. Distribution of Mycobacterium avium subsp. avium and M. a. hominissuis in artificially infected pigs studied by culture and IS901 and IS1245 quantitative real time PCR. Vet Microbiol. 2010;144(3-4):437-43.

  • 72. Klanicova B, Slana I, Vondruskova H, Kaevska M, Pavlik I. Real-Time Quantitative PCR Detection of Mycobacterium avium Subspecies in Meat Products. J Food Prot. 2011;74(4):636-40.

  • 73. Lorencova A, Vasickova P, Makovcova J, Slana I. Presence of Mycobacterium avium subspecies and hepatitis E virus in raw meat products. J Food Prot. 2014;77(2):335-8.

  • 74. Kaevska M, Lvoncik S, Slana I, Kulich P, Kralik P. Microscopy, culture, and quantitative real-time pcr examination confirm internalization of mycobacteria in plants. Appl Environ Microbiol. 2014;80(13):3888-94.

  • 75. Cvetkovikj I, Mrenoshki S, Krstevski K, Djadjovski I, Angjelovski B, Popova Z, Janevski A, Dodovski A, Cvetkovikj A. Bovine tuberculosis in the Republic of Macedonia: postmortem, microbiological and molecular study in slaughtered reactor cattle. Mac. Vet. Rev. 2017;40(1), doi: 10.1515/macvetrev-2016-0097.

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