Mycobacteriosis in Pigs – An Underrated Threat

1. Falkinham JO. Surrounded by mycobacteria: Nontuberculous mycobacteria in the human environment. J Appl Microbiol. 2009;107(2):356-67.10.1111/j.1365-2672.2009.04161.x19228258Search in Google Scholar

2. Falkinham JO. Nontuberculous Mycobacteria: Community and Nosocomial Waterborne Opportunistic Pathogens. Clin Microbiol Newsl. 2016;38(1):1-7.10.1016/j.clinmicnews.2015.12.003Search in Google Scholar

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;16:99-102.10.1016/j.meegid.2013.01.02223416257Search in Google Scholar

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):835-41.10.1016/j.meatsci.2014.08.00125170820Search in Google Scholar

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):1452-6.10.4315/0362-028X.JFP-16-03027497136Search in Google Scholar

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):141-4.10.4315/0362-028X.JFP-13-03624406012Search in Google Scholar

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):437-43.10.1016/j.vetmic.2010.02.02420227841Search in Google Scholar

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):83.10.1016/j.jcpa.2014.10.170Search in Google Scholar

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):941-8.10.1016/j.ijmm.2014.06.00125091874Search in Google Scholar

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):218-30.10.1016/j.jcpa.2016.06.00827426001Search in Google Scholar

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.Search in Google Scholar

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):227-30.10.1016/j.jcpa.2015.07.00126292770Search in Google Scholar

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;208:93-5.10.1016/j.tvjl.2015.10.00426639827Search in Google Scholar

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.Search in Google Scholar

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):1328-9.10.3201/eid1608.100097329829320678341Search in Google Scholar

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):372-7.10.1016/j.jcpa.2011.07.00821906752Search in Google Scholar

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):130.10.1186/s12917-015-0445-2446194426063469Search in Google Scholar

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):531-4.10.1177/104063871349068923780935Search in Google Scholar

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. 2016.10.1016/j.rvsc.2016.09.01327892873Search in Google Scholar

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):65-70.10.1111/lam.1224324612016Search in Google Scholar

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):911-34.10.1016/j.femsre.2005.02.00116219512Search in Google Scholar

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):1261-8.10.1128/JCM.43.3.1261-1268.2005108122715750094Search in Google Scholar

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):227-36.10.1016/j.vetmic.2004.06.00315327797Search in Google Scholar

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):247-55.10.1016/j.vetmic.2004.06.00515327799Search in Google Scholar

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):116-22.10.1111/j.0269-283X.2004.00477.x15189236Search in Google Scholar

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. 10.1155/2014/189649424128725431762Search in Google Scholar

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;45:46.10.1186/1297-9716-45-46402146524742183Search in Google Scholar

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):159.10.1186/1471-2180-9-159274146719660141Search in Google Scholar

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):202-16.10.1515/acve-2015-0017Search in Google Scholar

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):371-89.10.1515/acve-2015-0031Search in Google Scholar

31. Faria S, Joao I, Jordao L. General Overview on Nontuberculous Mycobacteria, Biofilms, and Human Infection. J Pathog. 2015;2015:1-10.10.1155/2015/809014464909326618006Search in Google Scholar

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

33. Rindi L, Garzelli C. Genetic diversity and phylogeny of Mycobacterium avium. Infect Genet Evol. 2014;21:375-83.10.1016/j.meegid.2013.12.00724345519Search in Google Scholar

34. Inderlied CB, Kemper CA, Bermudez LE. The Mycobacterium avium complex. Clin Microbiol Rev. 1993;6(3):266-310.10.1128/CMR.6.3.266Search in Google Scholar

35. Falkinham JO. Epidemiology of infection by nontuberculous mycobacteria . Epidemiology of Infection by Nontuberculous Mycobacteria. Clin Microbiol Rev. 1996;9(2):177-215.10.1128/CMR.9.2.177Search in Google Scholar

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):557-65.10.1016/S1473-3099(04)01130-2Search in Google Scholar

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):2915-23.10.1128/JCM.41.7.2915-2923.200316529112843021Search in Google Scholar

38. Grant IR. Zoonotic potential of Mycobacterium avium ssp. paratuberculosis: The current position. J Appl Microbiol. 2005;98(6):1282-93.10.1111/j.1365-2672.2005.02598.x15916642Search in Google Scholar

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.Search in Google Scholar

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.Search in Google Scholar

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):131-3.10.1016/j.jns.2013.09.01124075312Search in Google Scholar

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):185-8.10.1016/j.rvsc.2010.06.00920621319Search in Google Scholar

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. 10.1016/j.vetmic.2004.01.00815066726Search in Google Scholar

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;36:250-5.10.1016/j.meegid.2015.09.02926435330Search in Google Scholar

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):537-50.10.1016/j.cimid.2007.10.00218243315Search in Google Scholar

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):846-52.10.1016/j.meegid.2011.06.01821745597Search in Google Scholar

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;Search in Google Scholar

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):14-9.10.3103/S0891416814040119Search in Google Scholar

49. Andersen P, Doherty TM. The success and failure of BCG-implication for a novel tuberculosis vaccine. Nat Rev Microbiol. 2005;3:657-62.10.1038/nrmicro121116012514Search in Google Scholar

50. Andersen P. Tuberculosis vaccine- an update. Nat Rev Microbiol. 2007;5:484-7.10.1038/nrmicro170317571458Search in Google Scholar

51. Graham R, Stewart BDR a. DBY. Tuberculosis: A Problem with Persistence. Nat Rev Microbiol. 2003;1:97-105.10.1038/nrmicro74915035039Search in Google Scholar

52. Campbell IA. Opportunist (environmental) mycobacterial diseases. Medicine (Baltimore). 2008;36(6):306-8.10.1016/j.mpmed.2008.03.007Search in Google Scholar

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;7:63.10.1186/1746-6148-7-63321564322014189Search in Google Scholar

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.Search in Google Scholar

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.Search in Google Scholar

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):376-8.10.1177/104063871143514122362535Search in Google Scholar

57. Orme IM, Basaraba RJ. The formation of the granuloma in tuberculosis infection. Semin Immunol. 2014;26(6):601-9.10.1016/j.smim.2014.09.00925453231Search in Google Scholar

58. Ulrichs T, Kaufmann SHE. New insights into the function of granulomas in human tuberculosis. J Pathol. 2006;208(2):261-9.10.1002/path.190616362982Search in Google Scholar

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. 10.1016/j.jcpa.2012.05.005Search in Google Scholar

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):116-20.10.1136/vr.164.4.116Search in Google Scholar

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):143-50.10.1556/avet.52.2004.2.2Search in Google Scholar

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):815-7.10.7589/0090-3558-48.3.815Search in Google Scholar

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):930-40.10.1128/JCM.03168-14Search in Google Scholar

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.Search in Google Scholar

65. Monaghan,M.L., Doherty, M.L., Collins, J.D., Kazda, J.F., Quinn PJ. The tuberculin test. Veterinary Microbiology. 1994;40:111-24.10.1016/0378-1135(94)90050-7Search in Google Scholar

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):633-40.10.1002/path.172815776475Search in Google Scholar

67. K. Sakamoto. The Pathology of Mycobacterium tuberculosis Infection. Vet Pathol. 2012;49(3):423-39.10.1177/030098581142931322262351Search in Google Scholar

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;10.31274/ans_air-180814-701Search in Google Scholar

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):143-8.10.1017/S095026881000177920653991Search in Google Scholar

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):167-72.10.1128/JCM.00802-10302042121084514Search in Google Scholar

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):437-43.10.1016/j.vetmic.2010.02.02420227841Search in Google Scholar

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):636-40.10.4315/0362-028X.JFP-10-33221477480Search in Google Scholar

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):335-8.10.4315/0362-028X.JFP-13-25224490931Search in Google Scholar

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):3888-94.10.1128/AEM.00496-14405419824747896Search in Google Scholar

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. Search in Google Scholar