First report of Mycobacterium avium subsp. hominissuis in a black howler monkey (Alouatta caraya): a study with mycobacterial interspersed repetitive unit–variable number of tandem repeats genetic profiling

1. Barthel Y., Drews S., Fehr M., Moser I., Matz-Rensing K., Baumgärtner 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, 242–246, doi: 10.2376/0005-9366-129-15044. Barthel Y. Drews S. Fehr M. Moser I. Matz-Rensing K. Baumgärtner 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 , 242 – 246 , 10.2376/0005-9366-129-15044 . Open DOISearch in Google Scholar

2. Bermudez L., Yamazaki Y.: Effects of Macrolides and Ketolides on Mycobacterial Infections. Curr Pharm Des 2004, 10, 3221–3228, doi: 10.2174/1381612043383241. Bermudez L. Yamazaki Y. : Effects of Macrolides and Ketolides on Mycobacterial Infections . Curr Pharm Des 2004 , 10 , 3221 – 3228 , 10.2174/1381612043383241 . Open DOISearch in Google Scholar

3. Borek A., Zabost A., Głogowska A., Filipczak D., Augustynowicz-Kopeć E.: New RAPMYCOI Sensititre™ Antimicrobial Susceptibility Test for Atypical Rapidly Growing Mycobacteria (RGM). Diagnostics 2022, 12, 1976, doi: 10.3390/diagnostics12081976. Borek A. Zabost A. Głogowska A. Filipczak D. Augustynowicz-Kopeć E. : New RAPMYCOI Sensititre™ Antimicrobial Susceptibility Test for Atypical Rapidly Growing Mycobacteria (RGM) . Diagnostics 2022 , 12 , 1976 , 10.3390/diagnostics12081976 . Open DOISearch in Google Scholar

4. Brown-Elliott B.A., Nash K.A., Wallace R.J.: Antimicrobial Susceptibility Testing, Drug Resistance Mechanisms, and Therapy of Infections with Nontuberculous Mycobacteria. Clin Microbiol Rev 2012, 25, 545–582, doi: 10.1128/CMR.05030-11. Brown-Elliott B.A. Nash K.A. Wallace R.J. : Antimicrobial Susceptibility Testing, Drug Resistance Mechanisms, and Therapy of Infections with Nontuberculous Mycobacteria . Clin Microbiol Rev 2012 , 25 , 545 – 582 , 10.1128/CMR.05030-11 . Open DOISearch in Google Scholar

5. Bruczyńska M., Didkowska A., Brzezińska S., Nowak M., Filip-Hutsch K., Kalicki M., Augustynowicz-Kopeć E., Anusz K. Mycobacterium avium Subspecies paratuberculosis in Asymptomatic Zoo Herbivores in Poland. Animals 2023, 13, 1022, doi: 10.3390/ani13061022. Bruczyńska M. Didkowska A. Brzezińska S. Nowak M. Filip-Hutsch K. Kalicki M. Augustynowicz-Kopeć E. Anusz K. Mycobacterium avium Subspecies paratuberculosis in Asymptomatic Zoo Herbivores in Poland . Animals 2023 , 13 , 1022 , 10.3390/ani13061022 . Open DOISearch in Google Scholar

6. Clinical and Laboratory Standards Institute: M24-Ed3 Susceptibility Testing of Mycobacteria, Nocardia Spp., and Other Aerobic Actinomycetes; Approved Standard. CLSI, Wayne, PA, USA 2018. Clinical and Laboratory Standards Institute : M24-Ed3 Susceptibility Testing of Mycobacteria, Nocardia Spp., and Other Aerobic Actinomycetes; Approved Standard . CLSI , Wayne, PA, USA 2018 . Search in Google Scholar

7. Cochard T., Branger M., Supply P., Sreevatsan S., Biet F.: MAC-INMV-SSR: a web application dedicated to genotyping members of Mycobacterium avium complex (MAC) including Mycobacterium avium subsp. paratuberculosis strains. Infect Genet Evol 2020, 77, 104075, doi: 10.1016/j.meegid.2019.104075. Cochard T. Branger M. Supply P. Sreevatsan S. Biet F. : MAC-INMV-SSR: a web application dedicated to genotyping members of Mycobacterium avium complex (MAC) including Mycobacterium avium subsp. paratuberculosis strains . Infect Genet Evol 2020 , 77 , 104075 , 10.1016/j.meegid.2019.104075 . Open DOISearch in Google Scholar

8. Fechner K., Schäfer J., Münster P., Ternes K., Döring S., Völkel I., Kaup F.-J., Czerny C.-P.: Detection of Mycobacterium avium subspecies paratuberculosis in Rock Hyraxes (Procavia capensis) imported from South Africa. J Zoo Wildl Med 2017, 48, 1086–1094, doi: 10.1638/1042-7260-48.4.1086. Fechner K. Schäfer J. Münster P. Ternes K. Döring S. Völkel I. Kaup F.-J. Czerny C.-P. : Detection of Mycobacterium avium subspecies paratuberculosis in Rock Hyraxes (Procavia capensis) imported from South Africa . J Zoo Wildl Med 2017 , 48 , 1086 – 1094 , 10.1638/1042-7260-48.4.1086 . Open DOISearch in Google Scholar

9. Gałązka M., Didkowska A., Anusz K., Pyziel-Serafin A.: A review of tuberculosis and parasitic disease co-infection in ungulates, with regard to the potential threat to European bison (Bison bonasus). Polish J Vet Sci 2023, 155–161, doi: 10.24425/pjvs.2023.145018. Gałązka M. Didkowska A. Anusz K. Pyziel-Serafin A. : A review of tuberculosis and parasitic disease co-infection in ungulates, with regard to the potential threat to European bison (Bison bonasus) . Polish J Vet Sci 2023 , 155 – 161 , 10.24425/pjvs.2023.145018 . Open DOISearch in Google Scholar

10. Glawischnig W., Steineck T., Spergser J.: Infections caused by Mycobacterium avium subspecies avium, hominissuis, and paratuberculosis in free-ranging red deer (Cervus elaphus hippelaphus) in Austria, 2001–2004. J Wildl Dis 2006, 42, 724–731, doi: 10.7589/0090-3558-42.4.724. Glawischnig W. Steineck T. Spergser J. : Infections caused by Mycobacterium avium subspecies avium, hominissuis, and paratuberculosis in free-ranging red deer (Cervus elaphus hippelaphus) in Austria, 2001–2004 . J Wildl Dis 2006 , 42 , 724 – 731 , 10.7589/0090-3558-42.4.724 . Open DOISearch in Google Scholar

11. Gookin J. L., Stauffer S. H., Levy M. G.: Identification of Pentatrichomonas hominis in feline fecal samples by polymerase chain reaction assay. Vet Parasitol 2007, 145, 11–15. https://doi.org/10.1016/j.vetpar.2006.10.020. Gookin J. L. Stauffer S. H. Levy M. G. : Identification of Pentatrichomonas hominis in feline fecal samples by polymerase chain reaction assay . Vet Parasitol 2007 , 145 , 11 – 15 . https://doi.org/10.1016/j.vetpar.2006.10.020. Search in Google Scholar

12. Hamlen H.J., Lawrence J.M.: Giardiasis in laboratory-housed squirrel monkeys: a retrospective study. Lab Anim Sci 1994, 44, 235–239. Hamlen H.J. Lawrence J.M. : Giardiasis in laboratory-housed squirrel monkeys: a retrospective study . Lab Anim Sci 1994 , 44 , 235 – 239 . Search in Google Scholar

13. Ichikawa K., van Ingen J., Koh W.J., Wagner D., Salfinger M., Inagaki T., Uchiya K.I., 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, 250–255, doi: 10.1016/j.meegid.2015.09.029. Ichikawa K. van Ingen J. Koh W.J. Wagner D. Salfinger M. Inagaki T. Uchiya K.I. 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 – 255 , 10.1016/j.meegid.2015.09.029 . Open DOISearch in Google Scholar

14. 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, 846–852, doi: 10.1016/j.meegid.2011.06.018. 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 , 846 – 852 , 10.1016/j.meegid.2011.06.018 . Open DOISearch in Google Scholar

15. Kaczmarkowska A., Didkowska A., Kwiecień E., Stefańska I., Rzewuska M., Anusz K.: The Mycobacterium avium complex – an underestimated threat to humans and animals. Ann Agric Environ Med 2022, 29, 22–27, doi: 10.26444/aaem/136398. Kaczmarkowska A. Didkowska A. Kwiecień E. Stefańska I. Rzewuska M. Anusz K. : The Mycobacterium avium complex – an underestimated threat to humans and animals . Ann Agric Environ Med 2022 , 29 , 22 – 27 , 10.26444/aaem/136398 . Open DOISearch in Google Scholar

16. Krajewska M., Załuski M., Zabost A., Orłowska B., Augustynowicz-Kopeć E., Anusz K., Lipiec M., Weiner M., Szulowski K.: Tuberculosis in Antelopes in a Zoo in Poland – Problem of Public Health. Pol J Microbiol 2015, 64, 395–397, doi: 10.5604/17331331.1185242. Krajewska M. Załuski M. Zabost A. Orłowska B. Augustynowicz-Kopeć E. Anusz K. Lipiec M. Weiner M. Szulowski K. : Tuberculosis in Antelopes in a Zoo in Poland – Problem of Public Health . Pol J Microbiol 2015 , 64 , 395 – 397 , 10.5604/17331331.1185242 . Open DOISearch in Google Scholar

17. Krajewska-Wędzina M., Augustynowicz-Kopeć E., Weiner M., Szulowski K.: Treatment for active tuberculosis in giraffe (Giraffa camelopardalis) in a Zoo and potential consequences for public health – Case report. Ann Agric Environ Med 2018, 25, 593–595, doi: 10.26444/aaem/75685. Krajewska-Wędzina M. Augustynowicz-Kopeć E. Weiner M. Szulowski K. : Treatment for active tuberculosis in giraffe (Giraffa camelopardalis) in a Zoo and potential consequences for public health – Case report . Ann Agric Environ Med 2018 , 25 , 593 – 595 , 10.26444/aaem/75685 . Open DOISearch in Google Scholar

18. Lalle M., Pozio E., Capelli G., Bruschi F., Crotti D., Cacciò S.M.: Genetic heterogeneity at the β-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 2005, 35, 207–213, doi: 10.1016/j.ijpara.2004.10.022. Lalle M. Pozio E. Capelli G. Bruschi F. Crotti D. Cacciò S.M. : Genetic heterogeneity at the β-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes . Int J Parasitol 2005 , 35 , 207 – 213 , 10.1016/j.ijpara.2004.10.022 . Open DOISearch in Google Scholar

19. Majchrzak M., Kaczmarkowska A., Didkowska A., Brzezińska S., Orłowska B., Klich D., Augustynowicz-Kopeć E., Anusz K., Parniewski P.: MIRU-VNTR Typing of Atypical Mycobacteria Isolated from the Lymph Nodes of Slaughtered Pigs from Poland. Pathogens 2022, 11, 495, doi: 10.3390/pathogens11050495. Majchrzak M. Kaczmarkowska A. Didkowska A. Brzezińska S. Orłowska B. Klich D. Augustynowicz-Kopeć E. Anusz K. Parniewski P. : MIRU-VNTR Typing of Atypical Mycobacteria Isolated from the Lymph Nodes of Slaughtered Pigs from Poland . Pathogens 2022 , 11 , 495 , 10.3390/pathogens11050495 . Open DOISearch in Google Scholar

20. Martínez-Mota R., Kowalewski M.M., Gillespie T.R.: Chapter 10, Ecological Determinants of Parasitism in Howler Monkeys. In: Howler Monkeys, part of the Developments in Primatology: Progress and Prospects seriesedited by M.M. Kowalewski, P.A. Garber, L. Cortés-Ortiz, B. Urbani, D. Youlatos, Springer Science+Business Media, New York, NY, USA, 2015, pp. 259–285, doi: 10.1007/978-1-4939-1957-4_10. Martínez-Mota R. Kowalewski M.M. Gillespie T.R. : Chapter 10, Ecological Determinants of Parasitism in Howler Monkeys . In: Howler Monkeys, part of the Developments in Primatology: Progress and Prospects seriesedited by M.M. Kowalewski, P.A. Garber, L. Cortés-Ortiz, B. Urbani, D. Youlatos , Springer Science+Business Media , New York, NY, USA , 2015 , pp. 259 – 285 , 10.1007/978-1-4939-1957-4_10 . Open DOISearch in Google Scholar

21. McNabe M., Tennant R., Danelishvili L., Young L., Bermudez L.E.: Mycobacterium avium subsp hominissuis biofilm is composed of distinct phenotypes and influenced by the presence of antimicrobials. Clin Microbiol Infect 2011, 17, 697–703, doi: 10.1111/j.1469-0691.2010.03307.x. McNabe M. Tennant R. Danelishvili L. Young L. Bermudez L.E. : Mycobacterium avium subsp hominissuis biofilm is composed of distinct phenotypes and influenced by the presence of antimicrobials . Clin Microbiol Infect 2011 , 17 , 697 – 703 , 10.1111/j.1469-0691.2010.03307.x . Open DOISearch in Google Scholar

22. Radulski Ł., Kalicki M., Krajewska-Wędzina M., Lipiec M., Szulowski K.: Pulmonary mycobacteriosis of sitatunga antelope caused by M. avium ssp. hominissuis. Ann Agric Environ Med 2022, 29, 220–223, doi: 10.26444/aaem/145158. Radulski Ł. Kalicki M. Krajewska-Wędzina M. Lipiec M. Szulowski K. : Pulmonary mycobacteriosis of sitatunga antelope caused by M. avium ssp. hominissuis . Ann Agric Environ Med 2022 , 29 , 220 – 223 , 10.26444/aaem/145158 . Open DOISearch in Google Scholar

23. Rattaprasert P., Nitatsukprasert C., Thima K., Chavalitshewinkoon-Petmitr P.: Development of Nested PCR for Identification of Entamoeba Coli in Stool Samples. Research Square, 2021, doi: 10.21203/rs.3.rs-965132/v1. Rattaprasert P. Nitatsukprasert C. Thima K. Chavalitshewinkoon-Petmitr P. : Development of Nested PCR for Identification of Entamoeba Coli in Stool Samples . Research Square , 2021 , 10.21203/rs.3.rs-965132/v1 . Open DOISearch in Google Scholar

24. Reil I., Duvnjak S., Špičić S., Kompes G., Bagarić A., Ɖuras M., Gudan Kurilj A., Lukač M., Jelić M., Zdelar-Tuk M.: Isolation of Multidrug-Resistant Mycobacterium Avium Subsp. Avium from a Wild Eurasian Otter (Lutra Lutra). Antibiotics 2024, 13, 591, doi: 10.3390/antibiotics13070591. Reil I. Duvnjak S. Špičić S. Kompes G. Bagarić A. Ɖuras M. Gudan Kurilj A. Lukač M. Jelić M. Zdelar-Tuk M. : Isolation of Multidrug-Resistant Mycobacterium Avium Subsp. Avium from a Wild Eurasian Otter (Lutra Lutra) . Antibiotics 2024 , 13 , 591 , 10.3390/antibiotics13070591 . Open DOISearch in Google Scholar

25. Shoulah S.A., Oschmann A.M., Selim A., Semmler T., Schwarz C., Kamal E., Hamouda F., Galila E., Bitter W., Lewin A.: Environmental Mycobacterium avium subsp. hominissuis have a higher probability to act as a recipient in conjugation than clinical strains. Plasmid 2018, 95, 28–35, doi: 10.1016/j.plasmid.2018.01.003. Shoulah S.A. Oschmann A.M. Selim A. Semmler T. Schwarz C. Kamal E. Hamouda F. Galila E. Bitter W. Lewin A. : Environmental Mycobacterium avium subsp. hominissuis have a higher probability to act as a recipient in conjugation than clinical strains . Plasmid 2018 , 95 , 28 – 35 , 10.1016/j.plasmid.2018.01.003 . Open DOISearch in Google Scholar

26. Thibault V.C., Grayon M., Boschiroli M.L., Hubbans C., Overduin P., Stevenson K., Gutierrez M.C., Supply P., Biet F.: New Variable-Number Tandem-Repeat Markers for Typing Mycobacterium avium Subsp. Paratuberculosis and M. avium Strains: Comparison with IS900 and IS1245 Restriction Fragment Length Polymorphism Typing. J Clin Microbiol 2007, 45, 2404–2410, doi: 10.1128/JCM.00476-07. Thibault V.C. Grayon M. Boschiroli M.L. Hubbans C. Overduin P. Stevenson K. Gutierrez M.C. Supply P. Biet F. : New Variable-Number Tandem-Repeat Markers for Typing Mycobacterium avium Subsp. Paratuberculosis and M. avium Strains: Comparison with IS900 and IS1245 Restriction Fragment Length Polymorphism Typing . J Clin Microbiol 2007 , 45 , 2404 – 2410 , 10.1128/JCM.00476-07 . Open DOISearch in Google Scholar

27. Whittaker E., López-Varela E., Broderick C., Seddon J.A.: Examining the Complex Relationship Between Tuberculosis and Other Infectious Diseases in Children. Front Pediatr 2019, 7, 233, doi: 10.3389/fped.2019.00233. Whittaker E. López-Varela E. Broderick C. Seddon J.A. : Examining the Complex Relationship Between Tuberculosis and Other Infectious Diseases in Children . Front Pediatr 2019 , 7 , 233 , 10.3389/fped.2019.00233 . Open DOISearch in Google Scholar

28. World Organisation for Animal Health (OIE): Part 3, Chapter 3.1.17. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, 13th Edition, World Organisation for Animal Health (OIE), Paris, 2024, p. 7. World Organisation for Animal Health (OIE) : Part 3, Chapter 3.1.17 . In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals , 13 th Edition , World Organisation for Animal Health (OIE) , Paris , 2024 , p. 7 . Search in Google Scholar

29. Xiao L., Escalante L., Yang C., Sulaiman I., Escalante A.A., Montali R.J., Fayer R., Lal A.A.: Phylogenetic Analysis of Cryptosporidium Parasites Based on the Small-Subunit rRNA Gene Locus. Appl Environ Microbiol 1999, 65, 1578–1583, doi: 10.1128/AEM.65.4.1578-1583.1999. Xiao L. Escalante L. Yang C. Sulaiman I. Escalante A.A. Montali R.J. Fayer R. Lal A.A. : Phylogenetic Analysis of Cryptosporidium Parasites Based on the Small-Subunit rRNA Gene Locus . Appl Environ Microbiol 1999 , 65 , 1578 – 1583 , 10.1128/AEM.65.4.1578-1583.1999 . Open DOISearch in Google Scholar

30. Yamaba Y., Ito Y., Suzuki K., Kikuchi T., Ogawa K., Fujiuchi S., Hasegawa N., Kurashima A., Higuchi T., Uchiya K., Watanabe A., Niimi A.: Moxifloxacin resistance and genotyping of Mycobacterium avium and Mycobacterium intracellulare isolates in Japan. J Infect Chemother 2019, 25, 995–1000, doi: 10.1016/j.jiac.2019.05.028. Yamaba Y. Ito Y. Suzuki K. Kikuchi T. Ogawa K. Fujiuchi S. Hasegawa N. Kurashima A. Higuchi T. Uchiya K. Watanabe A. Niimi A. : Moxifloxacin resistance and genotyping of Mycobacterium avium and Mycobacterium intracellulare isolates in Japan . J Infect Chemother 2019 , 25 , 995 – 1000 , 10.1016/j.jiac.2019.05.028 . Open DOISearch in Google Scholar

31. Yoshida S., Araki T., Asai T., Tsuyuguchi K., Arikawa K., Iwamoto T., Nakajima C., Suzuki Y., Ohya K., Yanai T., Wada T., Yamamoto T.: Phylogenetic uniqueness of Mycobacterium avium subspecies hominissuis isolated from an abnormal pulmonary bovine case. Infect Genet Evol 2018, 62, 122–129, doi: 10.1016/j.meegid.2018.04.013. Yoshida S. Araki T. Asai T. Tsuyuguchi K. Arikawa K. Iwamoto T. Nakajima C. Suzuki Y. Ohya K. Yanai T. Wada T. Yamamoto T. : Phylogenetic uniqueness of Mycobacterium avium subspecies hominissuis isolated from an abnormal pulmonary bovine case . Infect Genet Evol 2018 , 62 , 122 – 129 , 10.1016/j.meegid.2018.04.013 . Open DOISearch in Google Scholar

32. Zajac A.M., Johnson J., King S.E.: Evaluation of the Importance of Centrifugation as a Component of Zinc Sulfate Fecal Flotation Examinations. J Am Anim Hosp Assoc 2002, 38, 221–224, doi: 10.5326/0380221. Zajac A.M. Johnson J. King S.E. : Evaluation of the Importance of Centrifugation as a Component of Zinc Sulfate Fecal Flotation Examinations . J Am Anim Hosp Assoc 2002 , 38 , 221 – 224 , 10.5326/0380221 . Open DOISearch in Google Scholar

33. Zebardast N., Haghighi A., Yeganeh F., Seyyed Tabaei S.J., Gharavi M.J., Fallahi S., Lasjerdi Z., Salehi N., Taghipour N., Kohansal C., Naderi F.: Application of Multiplex PCR for Detection and Differentiation of Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii. Iran J Parasitol 2014, 9, 466–473. Zebardast N. Haghighi A. Yeganeh F. Seyyed Tabaei S.J. Gharavi M.J. Fallahi S. Lasjerdi Z. Salehi N. Taghipour N. Kohansal C. Naderi F. : Application of Multiplex PCR for Detection and Differentiation of Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii . Iran J Parasitol 2014 , 9 , 466 – 473 . Search in Google Scholar