Genetic diversity of Mycobacterium avium subsp. hominissuis strains isolated from humans, pigs, and human living environment

Infection, Genetics and Evolution

Volumn 12, Issue 4, 2012, Pages 846-852

  Iwamoto, Tomotada ^a   Nakajima, Chie ^b   Nishiuchi, Yukiko ^c   Kato, Tomoko ^d   Yoshida, Shiomi ^e   Nakanishi, Noriko ^a   Tamaru, Aki ^f   Tamura, Yutaka ^g   Suzuki, Yasuhiko ^b   Nasu, Masao ^d  

^a KOBE INSTITUTE OF HEALTH   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e NATIONAL HOSPITAL ORGANIZATION KINKI CHUO CHEST MEDICAL CENTER   (Japan)

^f OSAKA PREFECTURAL INSTITUTE OF PUBLIC HEALTH   (Japan)

^g RAKUNO GAKUEN UNIVERSITY   (Japan)

Author keywords

Genetic diversity; Insertion sequence; Minimum spanning tree; Molecular epidemiology; Mycobacterium avium subsp. hominissuis; Variable numbers of tandem repeat

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; FINLAND; FRANCE; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HSP65 GENE; JAPAN; MYCOBACTERIUM AVIUM; MYCOBACTERIUM HOMINISSUIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; VARIABLE NUMBER OF TANDEM REPEAT;

ALLELES; ANIMALS; BACTERIAL PROTEINS; CHAPERONIN 60; DNA, BACTERIAL; GENETIC VARIATION; HUMANS; MINISATELLITE REPEATS; MOLECULAR TYPING; MYCOBACTERIUM AVIUM; PHYLOGENY; PHYLOGEOGRAPHY; SWINE;

MYCOBACTERIUM AVIUM; SUIDAE;

EID: 84859913563     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2011.06.018     Document Type: Article

References (59)

1. Allix-Beguec C., Harmsen D., Weniger T., Supply P., Niemann S. Evaluation and strategy for use of MIRU-VNTRplus, a multifunctional database for online analysis of genotyping data and phylogenetic identification of Mycobacterium tuberculosis complex isolates. J. Clin. Microbiol. 2008, 46:2692-2699.
2. Angenent L.T., Kelley S.T., St Amand A., Pace N.R., Hernandez M.T. Molecular identification of potential pathogens in water and air of a hospital therapy pool. Proc. Natl. Acad. Sci. USA 2005, 102:4860-4865.
3. Aronson T., Holtzman A., Glover N., Boian M., Froman S., Berlin O.G., Hill H., Stelma G. Comparison of large restriction fragments of Mycobacterium avium isolates recovered from AIDS and non-AIDS patients with those of isolates from potable water. J. Clin. Microbiol. 1999, 37:1008-1012.
4. Biet F., Boschiroli M.L., Thorel M.F., Guilloteau L.A. Zoonotic aspects of Mycobacterium bovis and Mycobacterium avium-intracellulare complex (MAC). Vet. Res. 2005, 36:411-436.
5. Cayrou C., Turenne C., Behr M.A., Drancourt M. Genotyping of Mycobacterium avium complex organisms using multispacer sequence typing. Microbiology 2010, 156:687-694.
6. du Moulin G.C., Stottmeier K.D., Pelletier P.A., Tsang A.Y., Hedley-Whyte J. Concentration of Mycobacterium avium by hospital hot water systems. JAMA 1988, 260:1599-1601.
7. Embil J., Warren P., Yakrus M., Stark R., Corne S., Forrest D., Hershfield E. Pulmonary illness associated with exposure to Mycobacterium-avium complex in hot tub water. Hypersensitivity pneumonitis or infection?. Chest 1997, 111:813-816.
8. Falkinham J.O. Impact of human activities on the ecology of nontuberculous mycobacteria. Future Microbiol. 2010, 5:951-960.
9. Falkinham J.O. Epidemiology of infection by nontuberculous mycobacteria. Clin. Microbiol. Rev. 1996, 9:177-215.
10. Falkinham J.O., Iseman M.D., de Haas P., van Soolingen D. Mycobacterium avium in a shower linked to pulmonary disease. J. Water Health 2008, 6:209-213.
11. Feazel L.M., Baumgartner L.K., Peterson K.L., Frank D.N., Harris J.K., Pace N.R. Opportunistic pathogens enriched in showerhead biofilms. Proc. Natl. Acad. Sci. USA 2009, 106:16393-16399.
12. Glassroth J. Pulmonary disease due to nontuberculous mycobacteria. Chest 2008, 133:243-251.
13. Hanekom M., van der Spuy G.D., Streicher E., Ndabambi S.L., McEvoy C.R., Kidd M., Beyers N., Victor T.C., van Helden P.D., Warren R.M. A recently evolved sublineage of the Mycobacterium tuberculosis Beijing strain family is associated with an increased ability to spread and cause disease. J. Clin. Microbiol. 2007, 45:1483-1490.
14. Hibiya K., Utsunomiya K., Yoshida T., Toma S., Higa F., Tateyama M., Fujita J. Pathogenesis of systemic Mycobacterium avium infection in pigs through histological analysis of hepatic lesions. Can. J. Vet. Res. 2010, 74:252-257.
15. Hilborn E.D., Yakrus M.A., Covert T.C., Harris S.I., Donnelly S.F., Schmitt M.T., Toney S., Bailey S.A., Stelma G.N. Molecular comparison of Mycobacterium avium isolates from clinical and environmental sources. Appl. Environ. Microbiol. 2008, 74:4966-4968.
16. Hunter P.R., Gaston M.A. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J. Clin. Microbiol. 1988, 26:2465-2466.
17. Ichikawa K., Yagi T., Moriyama M., Inagaki T., Nakagawa T., Uchiya K., Nikai T., Ogawa K. Characterization of Mycobacterium avium clinical isolates in Japan using subspecies-specific insertion sequences, and identification of a new insertion sequence, ISMav6. J. Med. Microbiol. 2009, 58:945-950.
18. Inagaki T., Nishimori K., Yagi T., Ichikawa K., Moriyama M., Nakagawa T., Shibayama T., Uchiya K., Nikai T., Ogawa K. Comparison of a variable-number tandem-repeat (VNTR) method for typing Mycobacterium avium with mycobacterial interspersed repetitive-unit-VNTR and IS1245 restriction fragment length polymorphism typing. J. Clin. Microbiol. 2009, 47:2156-2164.
19. Iwamoto T., Tani K., Nakamura K., Suzuki Y., Kitagawa M., Eguchi M., Nasu M. Monitoring impact of in situ biostimulation treatment on groundwater bacterial community by DGGE. FEMS Microbiol. Ecol. 2000, 32:129-141.
20. Johansen T.B., Olsen I., Jensen M.R., Dahle U.R., Holstad G., Djonne B. New probes used for IS1245 and IS1311 restriction fragment length polymorphism of Mycobacterium avium subsp. avium and Mycobacterium avium subsp. hominissuis isolates of human and animal origin in Norway. BMC Microbiol. 2007, 7:14.
21. Kahana L.M., Kay J.M., Yakrus M.A., Waserman S. Mycobacterium avium complex infection in an immunocompetent young adult related to hot tub exposure. Chest 1997, 111:242-245.
22. Kang H.Y., Wada T., Iwamoto T., Maeda S., Murase Y., Kato S., Kim H.J., Park Y.K. Phylogeographical particularity of the Mycobacterium tuberculosis Beijing family in South Korea based on international comparison with surrounding countries. J. Med. Microbiol. 2010, 59:1191-1197.
23. Keim P., Price L.B., Klevytska A.M., Smith K.L., Schupp J.M., Okinaka R., Jackson P.J., Hugh-Jones M.E. Multiple-locus variable-number tandem repeat analysis reveals genetic relationships within Bacillus anthracis. J. Bacteriol. 2000, 182:2928-2936.
24. Kikuchi T., Watanabe A., Gomi K., Sakakibara T., Nishimori K., Daito H., Fujimura S., Tazawa R., Inoue A., Ebina M., Tokue Y., Kaku M., Nukiwa T. Association between mycobacterial genotypes and disease progression in Mycobacterium avium pulmonary infection. Thorax 2009, 64:901-907.
25. Komijn R.E., de Haas P.E., Schneider M.M., Eger T., Nieuwenhuijs J.H., van den Hoek R.J., Bakker D., van Zijd Erveld F.G., van Soolingen D. Prevalence of Mycobacterium avium in slaughter pigs in The Netherlands and comparison of IS1245 restriction fragment length polymorphism patterns of porcine and human isolates. J. Clin. Microbiol. 1999, 37:1254-1259.
26. Maeda S., Wada T., Iwamoto T., Murase Y., Mitarai S., Sugawara I., Kato S. Beijing family Mycobacterium tuberculosis isolated from throughout Japan: phylogeny and genetic features. Int. J. Tuberc. Lung Dis. 2010, 14:1201-1204.
27. Maekura R., Okuda Y., Hirotani A., Kitada S., Hiraga T., Yoshimura K., Yano I., Kobayashi K., Ito M. Clinical and prognostic importance of serotyping Mycobacterium avium-Mycobacterium intracellulare complex isolates in human immunodeficiency virus-negative patients. J. Clin. Microbiol. 2005, 43:3150-3158.
28. Mangione E.J., Huitt G., Lenaway D., Beebe J., Bailey A., Figoski M., Rau M.P., Albrecht K.D., Yakrus M.A. Nontuberculous mycobacterial disease following hot tub exposure. Emerg. Infect. Dis. 2001, 7:1039-1042.
29. Mijs W., de Haas P., Rossau R., Van der Laan T., Rigouts L., Portaels F., van Soolingen D. Molecular evidence to support a proposal to reserve the designation Mycobacterium avium subsp. avium for bird-type isolates and 'M. avium subsp. hominissuis' for the human/porcine type of M. avium. Int. J. Syst. Evol. Microbiol. 2002, 52:1505-1518.
30. Mobius P., Lentzsch P., Moser I., Naumann L., Martin G., Kohler H. Comparative macrorestriction and RFLP analysis of Mycobacterium avium subsp. avium and Mycobacterium avium subsp. hominissuis isolates from man, pig, and cattle. Vet. Microbiol. 2006, 117:284-291.
31. Mokrousov I. Towards a quantitative perception of human-microbial co-evolution. Front Biosci. 2007, 12:4818-4825.
32. Mokrousov I. Genetic geography of Mycobacterium tuberculosis Beijing genotype: a multifacet mirror of human history?. Infect. Genet. Evol. 2008, 8:777-785.
33. Mokrousov I., Ly H.M., Otten T., Lan N.N., Vyshnevskyi B., Hoffner S., Narvskaya O. Origin and primary dispersal of the Mycobacterium tuberculosis Beijing genotype: clues from human phylogeography. Genome Res. 2005, 15:1357-1364.
34. Mokrousov I., Narvskaya O., Otten T., Vyazovaya A., Limeschenko E., Steklova L., Vyshnevskyi B. Phylogenetic reconstruction within Mycobacterium tuberculosis Beijing genotype in northwestern Russia. Res. Microbiol. 2002, 153:629-637.
35. Mokrousov I., Narvskaya O., Vyazovaya A., Millet J., Otten T., Vishnevsky B., Rastogi N. Mycobacterium tuberculosis Beijing genotype in Russia: in search of informative variable-number tandem-repeat loci. J. Clin. Microbiol. 2008, 46:3576-3584.
36. Nishiuchi Y., Maekura R., Kitada S., Tamaru A., Taguri T., Kira Y., Hiraga T., Hirotani A., Yoshimura K., Miki M., Ito M. The recovery of Mycobacterium avium-intracellulare complex (MAC) from the residential bathrooms of patients with pulmonary MAC. Clin. Infect. Dis. 2007, 45:347-351.
37. Nishiuchi Y., Tamura A., Kitada S., Taguri T., Matsumoto S., Tateishi Y., Yoshimura M., Ozeki Y., Matsumura N., Ogura H., Maekura R. Mycobacterium avium complex organisms predominantly colonize in the bathtub inlets of patients' bathrooms. Jpn. J. Infect. Dis. 2009, 62:182-186.
38. Parker B.C., Ford M.A., Gruft H., Falkinham J.O. Epidemiology of infection by nontuberculous mycobacteria. IV. Preferential aerosolization of Mycobacterium intracellulare from natural waters. Am. Rev. Respir. Dis. 1983, 128:652-656.
39. Pate, M., Kusar, D., Zolnir-Dovc, M., Ocepek, M., 2010. MIRU-VNTR typing of Mycobacterium avium in animals and humans: heterogeneity of Mycobacterium avium subsp. hominissuis versus homogeneity of Mycobacterium avium subsp. avium strains. Res. Vet. Sci. doi:10.1016/j.rvsc.2010.10.001.
40. Petrini B. Non-tuberculous mycobacterial infections. Scand. J. Infect. Dis. 2006, 38:246-255.
41. Prevots D.R., Shaw P.A., Strickland D., Jackson L.A., Raebel M.A., Blosky M.A., Montes de Oca R., Shea Y.R., Seitz A.E., Holland S.M., Olivier K.N. Nontuberculous mycobacterial lung disease prevalence at four integrated health care delivery systems. Am. J. Respir. Crit. Care Med. 2010, 182:970-976.
42. Primm T.P., Lucero C.A., Falkinham J.O. Health impacts of environmental mycobacteria. Clin. Microbiol. Rev. 2004, 17:98-106.
43. Radomski N., Thibault V.C., Karoui C., de Cruz K., Cochard T., Gutierrez C., Supply P., Biet F., Boschiroli M.L. Determination of genotypic diversity of Mycobacterium avium subspecies from human and animal origins by mycobacterial interspersed repetitive-unit-variable-number tandem-repeat and IS1311 restriction fragment length polymorphism typing methods. J. Clin. Microbiol. 2010, 48:1026-1034.
44. Ramasoota P., Chansiripornchai N., Kallenius G., Hoffner S.E., Svenson S.B. Comparison of Mycobacterium avium complex (MAC) strains from pigs and humans in Sweden by random amplified polymorphic DNA (RAPD) using standardized reagents. Vet. Microbiol. 2001, 78:251-259.
45. Sakatani M. Nontuberculous mycobacteriosis; the present status of epidemiology and clinical studies. Kekkaku 1999, 74:377-384.
46. Supply P., Mazars E., Lesjean S., Vincent V., Gicquel B., Locht C. Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol. Microbiol. 2000, 36:762-771.
47. Supply P., Warren R.M., Banuls A.L., Lesjean S., Van Der Spuy G.D., Lewis L.A., Tibayrenc M., Van Helden P.D., Locht C. Linkage disequilibrium between minisatellite loci supports clonal evolution of Mycobacterium tuberculosis in a high tuberculosis incidence area. Mol. Microbiol. 2003, 47:529-538.
48. Taylor R.H., Falkinham J.O., Norton C.D., LeChevallier M.W. Chlorine, chloramine, chlorine dioxide, and ozone susceptibility of Mycobacterium avium. Appl. Environ. Microbiol. 2000, 66:1702-1705.
49. 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.
50. Tirkkonen T., Pakarinen J., Moisander A.M., Makinen J., Soini H., Ali-Vehmas T. High genetic relatedness among Mycobacterium avium strains isolated from pigs and humans revealed by comparative IS1245 RFLP analysis. Vet. Microbiol. 2007, 125:175-181.
51. Tirkkonen T., Pakarinen J., Rintala E., Ali-Vehmas T., Marttila H., Peltoniemi O.A., Makinen J. Comparison of variable-number tandem-repeat markers typing and IS1245 restriction fragment length polymorphism fingerprinting of Mycobacterium avium subsp. hominissuis from human and porcine origins. Acta Vet. Scand. 2010, 52:21.
52. Turenne C.Y., Semret M., Cousins D.V., Collins D.M., Behr M.A. Sequencing of hsp65 distinguishes among subsets of the Mycobacterium avium complex. J. Clin. Microbiol. 2006, 44:433-440.
53. Turenne C.Y., Wallace R., Behr M.A. Mycobacterium avium in the postgenomic era. Clin. Microbiol. Rev. 2007, 20:205-229.
54. von Reyn C.F., Maslow J.N., Barber T.W., Falkinham J.O., Arbeit R.D. Persistent colonisation of potable water as a source of Mycobacterium avium infection in AIDS. Lancet 1994, 343:1137-1141.
55. Wada T., Iwamoto T. Allelic diversity of variable number of tandem repeats provides phylogenetic clues regarding the Mycobacterium tuberculosis Beijing family. Infect. Genet. Evol. 2009, 9:921-926.
56. Wada T., Iwamoto T., Maeda S. Genetic diversity of the Mycobacterium tuberculosis Beijing family in East Asia revealed through refined population structure analysis. FEMS Microbiol. Lett. 2009, 291:35-43.
57. Wendt S.L., George K.L., Parker B.C., Gruft H., Falkinham J.O. Epidemiology of infection by nontuberculous Mycobacteria. III. Isolation of potentially pathogenic mycobacteria from aerosols. Am. Rev. Respir. Dis. 1980, 122:259-263.
58. Winthrop K.L. Pulmonary disease due to nontuberculous mycobacteria: an epidemiologist's view. Future Microbiol. 2010, 5:343-345.
59. Wirth T., Hildebrand F., Allix-Beguec C., Wolbeling F., Kubica T., Kremer K., van Soolingen D., Rusch-Gerdes S., Locht C., Brisse S., Meyer A., Supply P., Niemann S. Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog. 2008, 4:e1000160.