Towards the molecular epidemiology of Mycobacterium leprae: Strategies, successes, and shortcomings

Infection, Genetics and Evolution

Volumn 11, Issue 7, 2011, Pages 1505-1513

  Salipante, Stephen J ^a,b   Hall, Barry G ^a  

^a Bellingham Research Institute   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Leprosy; Molecular epidemiology; Mycobacterium leprae

Indexed keywords

BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; DISEASE CARRIER; GENETIC ALGORITHM; GENETIC MARKER; HUMAN; LEPROSY; MATHEMATICAL MODEL; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; MULTILOCUS SEQUENCE TYPING; MYCOBACTERIUM LEPRAE; NONHUMAN; PHYLOGENY; POLYMORPHIC LOCUS; POPULATION GENETIC STRUCTURE; PRIORITY JOURNAL; PROCESS DEVELOPMENT; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; VARIABLE NUMBER OF TANDEM REPEAT;

BACTERIAL TYPING TECHNIQUES; DISEASE RESERVOIRS; ENVIRONMENTAL MICROBIOLOGY; GENES, BACTERIAL; HUMANS; LEPROSY; MINISATELLITE REPEATS; MOLECULAR EPIDEMIOLOGY; MYCOBACTERIUM LEPRAE; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM LEPRAE;

EID: 80053570886     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2011.06.003     Document Type: Review

References (86)

1. Abide J.M., Webb R.M., Jones H.L., Young L. Three indigenous cases of leprosy in the Mississippi delta. South Med J 2008, 101:635-638.
2. Achtman M. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu. Rev. Microbiol. 2008, 62:53-70.
3. Ahmed R., Bopp C., Borczyk A., Kasatiya S. Phage-typing scheme for Escherichia coli O157:H7. J Infect Dis 1987, 155:806-809.
4. Amezcua M.E., Escobar-Gutierrez A., Storrs E.E., Dhople A.M., Burchfield H.P. Wild Mexican armadillo with leprosy-like infection. Int. J. Lepr. Other Mycobact. Dis. 1984, 52:254-255.
5. Anon. Global leprosy situation, 2010. Wkly. Epidemiol. Rec. 2010, 85:337-348.
6. Arbeit R.D., Arthur M., Dunn R., Kim C., Selander R.K., Goldstein R. Resolution of recent evolutionary divergence among Escherichia coli from related lineages: the application of pulsed field electrophoresis to molecular epidemiology. J. Infect. Dis. 1990, 161:230-235.
7. Boyer J.C., Yamada N.A., Roques C.N., Hatch S.B., Riess K., Farber R.A. Sequence dependent instability of mononucleotide microsatellites in cultured mismatch repair proficient and deficient mammalian cells. Hum. Mol. Genet. 2002, 11:707-713.
8. Cardona-Castro N., Beltran J.C., Ortiz-Bernal A., Vissa V. Detection of Mycobacterium leprae DNA in nine-banded armadillos (Dasypus novemcinctus) from the Andean region of Colombia. Lepr. Rev. 2009, 80:424-431.
9. Cardona-Castro N., Beltran-Alzate J.C., Romero-Montoya I.M., Melendez E., Torres F., Sakamuri R.M., Li W., Vissa V. Identification and comparison of Mycobacterium leprae genotypes in two geographical regions of Colombia. Lepr. Rev. 2009, 80:316-321.
10. Chae G.T., Lee S.B., Kang T.J., Shin H.K., Kim J.P., Ko Y.H., Kim S.H., Kim N.H. Typing of clinical isolates of Mycobacterium leprae and their distribution in Korea. Lepr. Rev. 2002, 73:41-46.
11. Cho S.N., Kim S.H., Cellona R.V., Chan G.P., Fajardo T.T., Walsh G.P., Kim J.D. Prevalence of IgM antibodies to phenolic glycolipid I among household contacts and controls in Korea and the Philippines. Lepr. Rev. 1992, 63:12-20.
12. Clark-Curtiss J.E., Walsh G.P. Conservation of genomic sequences among isolates of Mycobacterium leprae. J. Bacteriol. 1989, 171:4844-4851.
13. Cole S.T., Eiglmeier K., Parkhill J., James K.D., Thomson N.R., Wheeler P.R., Honore N., Garnier T., Churcher C., Harris D., Mungall K., Basham D., Brown D., Chillingworth T., Connor R., Davies R.M., Devlin K., Duthoy S., Feltwell T., Fraser A., Hamlin N., Holroyd S., Hornsby T., Jagels K., Lacroix C., Maclean J., Moule S., Murphy L., Oliver K., Quail M.A., Rajandream M.A., Rutherford K.M., Rutter S., Seeger K., Simon S., Simmonds M., Skelton J., Squares R., Squares S., Stevens K., Taylor K., Whitehead S., Woodward J.R., Barrell B.G. Massive gene decay in the leprosy bacillus. Nature 2001, 409:1007-1011.
14. Cole S.T., Supply P., Honore N. Repetitive sequences in Mycobacterium leprae and their impact on genome plasticity. Lepr. Rev. 2001, 72:449-461.
15. Comas I., Homolka S., Niemann S., Gagneux S. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS One 2009, 4:e7815.
16. de Wit M.Y., Klatser P.R. Mycobacterium leprae isolates from different sources have identical sequences of the spacer region between the 16S and 23S ribosomal RNA genes. Microbiology 1994, 140(Pt 8):1983-1987.
17. Deps P.D., Alves B.L., Gripp C.G., Aragao R.L., Guedes B., Filho J.B., Andreatta M.K., Marcari R.S., Prates I., Rodrigues L.C. Contact with armadillos increases the risk of leprosy in Brazil: a case control study. Indian J. Dermatol. Venereol. Leprol. 2008, 74:338-342.
18. Diamant E., Palti Y., Gur-Arie R., Cohen H., Hallerman E.M., Kashi Y. Phylogeny and strain typing of Escherichia coli, inferred from variation at mononucleotide repeat loci. Appl. Environ. Microbiol. 2004, 70:2464-2473.
19. Falush D., Wirth T., Linz B., Pritchard J.K., Stephens M., Kidd M., Blaser M.J., Graham D.Y., Vacher S., Perez-Perez G.I., Yamaoka Y., Megraud F., Otto K., Reichard U., Katzowitsch E., Wang X., Achtman M., Suerbaum S. Traces of human migrations in Helicobacter pylori populations. Science 2003, 299:1582-1585.
20. Feil E.J., Li B.C., Aanensen D.M., Hanage W.P., Spratt B.G. EBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 2004, 186:1518-1530.
21. Fine P.E. Leprosy: the epidemiology of a slow bacterium. Epidemiol. Rev. 1982, 4:161-188.
22. Fontes A.N., Sakamuri R.M., Baptista I.M., Ura S., Moraes M.O., Martinez A.N., Sarno E.N., Brennan P.J., Vissa V.D., Suffys P.N. Genetic diversity of Mycobacterium leprae isolates from Brazilian leprosy patients. Lepr. Rev. 2009, 80:302-315.
23. Gillis T., Vissa V., Matsuoka M., Young S., Richardus J.H., Truman R., Hall B., Brennan P. Characterisation of short tandem repeats for genotyping Mycobacterium leprae. Lepr. Rev. 2009, 80:250-260.
24. Graham R.L., Hell P. On the history of the minimum spanning tree problem. Ann. Hist. Comput. 1985, 7:43-57.
25. Groathouse N.A., Rivoire B., Kim H., Lee H., Cho S.N., Brennan P.J., Vissa V.D. Multiple polymorphic loci for molecular typing of strains of Mycobacterium leprae. J. Clin. Microbiol. 2004, 42:1666-1672.
26. Hall B.G. Phylogenetic Trees Made Easy: A How-To Manual 2011, Sinauer Assoc., Sunderland, MA. fourth ed. and third ed.
27. Hall B.G., Ehrlich G.D., Hu F.Z. Pan-genome analysis provides much higher strain typing resolution than multi-locus sequence typing. Microbiology 2010, 156:1060-1068.
28. Hall B.G., Salipante S.J. Molecular epidemiology of Mycobacterium leprae as determined by structure-neighbor clustering. J. Clin. Microbiol. 2010, 48:1997-2008.
29. Irgens L.M. The discovery of the leprosy bacillus. Tidsskr. Nor Laegeforen 2002, 122:708-709.
30. Izumi S., Budiawan T., Saeki K., Matsuoka M., Kawatsu K. An epidemiological study on Mycobacterium leprae infection and prevalence of leprosy in endemic villages by molecular biological technique. Indian J. Lepr. 1999, 71:37-43.
31. 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.
32. Kerr-Pontes L.R., Barreto M.L., Evangelista C.M., Rodrigues L.C., Heukelbach J., Feldmeier H. Socioeconomic, environmental, and behavioural risk factors for leprosy in North-east Brazil: results of a case-control study. Int. J. Epidemiol. 2006, 35:994-1000.
33. Kimura M., Sakamuri R.M., Groathouse N.A., Rivoire B.L., Gingrich D., Krueger-Koplin S., Cho S.N., Brennan P.J., Vissa V. Rapid variable-number tandem-repeat genotyping for Mycobacterium leprae clinical specimens. J. Clin. Microbiol. 2009, 47:1757-1766.
34. Kirchheimer W.F., Storrs E.E. Attempts to establish the armadillo (Dasypus novemcinctus Linn.) as a model for the study of leprosy. I. Report of lepromatoid leprosy in an experimentally infected armadillo. Int. J. Lepr. Other Mycobact. Dis. 1971, 39:693-702.
35. Kirchheimer W.F., Storrs E.E., Binford C.H. Attempts to establish the Armadillo (Dasypus novemcinctus linn.) as a model for the study of leprosy. II. Histopathologic and bacteriologic post-mortem findings in lepromatoid leprosy in the Armadillo. Int. J. Lepr. Other Mycobact. Dis. 1972, 40:229-242.
36. Klevytska A.M., Price L.B., Schupp J.M., Worsham P.L., Wong J., Keim P. Identification and characterization of variable-number tandem repeats in the Yersinia pestis genome. J. Clin. Microbiol. 2001, 39:3179-3185.
37. Lancefield R.C. The antigenic complex of Streptococcus haemolyticus: I. Demonstration of a type-specific substance in extracts of Streptococcus haemolyticus. J. Exp. Med. 1928, 47:91-103.
38. Leininger J.R., Donham K.J., Rubino M.J., Meyers W.M. Naturally acquired leprosy in a chimpanzee necropsy findings and experimental transmission to other animals. Lab. Invest. 1980, 42:132.
39. Low D.A., Braaten B.A., Ling G.V., Johnson D.L., Ruby A.L. Isolation and comparison of Escherichia coli strains from canine and human patients with urinary tract infections. Infect. Immun. 1988, 56:2601-2609.
40. Maiden M.C., Bygraves J.A., Feil E., Morelli G., Russell J.E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D.A., Feavers I.M., Achtman M., Spratt B.G. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 1998, 95:3140-3145.
41. Matsuoka M., Gonzalez A.V., Estrada I., Carreno-Martinez C., Fafutis-Morris M. Various genotypes of Mycobacterium leprae from Mexico reveal distinct geographic distribution. Lepr. Rev. 2009, 80:322-326.
42. Matsuoka M., Maeda S., Kai M., Nakata N., Chae G.T., Gillis T.P., Kobayashi K., Izumi S., Kashiwabara Y. Mycobacterium leprae typing by genomic diversity and global distribution of genotypes. Int. J. Lepr. Other Mycobact. Dis. 2000, 68:121-128.
43. Matsuoka M., Roa R.I., Budiawan T., Kyaw K., Chae G.T. Genotypic analysis of Mycobacterium leprae isolates from Japan and other Asian countries reveals a global transmission pattern of leprosy. FEMS Microbiol. Lett. 2006, 261:150-154.
44. Matsuoka M., Zhang L., Budiawan T., Saeki K., Izumi S. Genotyping of Mycobacterium leprae on the basis of the polymorphism of TTC repeats for analysis of leprosy transmission. J. Clin. Microbiol. 2004, 42:741-745.
45. Matsuoka M., Zhang L., Morris M.F., Legua P., Wiens C. Polymorphism in the rpoT gene in Mycobacterium leprae isolates obtained from Latin American countries and its possible correlation with the spread of leprosy. FEMS Microbiol. Lett. 2005, 243:311-315.
46. Mazars E., Lesjean S., Banuls A.L., Gilbert M., Vincent V., Gicquel B., Tibayrenc M., Locht C., Supply P. High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology. Proc. Natl. Acad. Sci. USA 2001, 98:1901-1906.
47. Meyers W.M., Gormus B.J., Walsh G.P. Nonhuman sources of leprosy. Int. J. Lepr. Other Mycobact. Dis. 1992, 60:477-480.
48. Meyers W.M., Gormus B.J., Walsh G.P., Baskin G.B., Hubbard G.B. Naturally acquired and experimental leprosy in nonhuman primates. Am. J. Trop. Med. Hyg. 1991, 44:24-27.
49. Milkman R. Electrophoretic variation in Escherichia coli from natural sources. Science 1973, 182:1024-1026.
50. Monot M., Honore N., Baliere C., Ji B., Sow S., Brennan P.J., Cole S.T. Are variable-number tandem repeats appropriate for genotyping Mycobacterium leprae?. J. Clin. Microbiol. 2008, 46:2291-2297.
51. Monot M., Honore N., Garnier T., Araoz R., Coppee J.Y., Lacroix C., Sow S., Spencer J.S., Truman R.W., Williams D.L., Gelber R., Virmond M., Flageul B., Cho S.N., Ji B., Paniz-Mondolfi A., Convit J., Young S., Fine P.E., Rasolofo V., Brennan P.J., Cole S.T. On the origin of leprosy. Science 2005, 308:1040-1042.
52. Monot M., Honore N., Garnier T., Zidane N., Sherafi D., Paniz-Mondolfi A., Matsuoka M., Taylor G.M., Donoghue H.D., Bouwman A., Mays S., Watson C., Lockwood D., Khamesipour A., Dowlati Y., Jianping S., Rea T.H., Vera-Cabrera L., Stefani M.M., Banu S., Macdonald M., Sapkota B.R., Spencer J.S., Thomas J., Harshman K., Singh P., Busso P., Gattiker A., Rougemont J., Brennan P.J., Cole S.T. Comparative genomic and phylogeographic analysis of Mycobacterium leprae. Nat. Genet. 2009, 41:1282-1289.
53. Musser J.M. Molecular population genetic analysis of emerged bacterial pathogens: selected insights. Emerg. Infect. Dis. 1996, 2:1-17.
54. Pedrini S.C., Rosa P.S., Medri I.M., Mourao G., Bagagli E., Lopes C.A. Search for Mycobacterium leprae in wild mammals. Braz. J. Infect. Dis. 2010, 14:47-53.
55. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
56. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
57. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
58. Sakamuri R.M., Harrison J., Gelber R., Saunderson P., Brennan P.J., Balagon M., Vissa V. A continuation: study and characterisation of Mycobacterium leprae short tandem repeat genotypes and transmission of leprosy in Cebu, Philippines. Lepr. Rev. 2009, 80:272-279.
59. Sakamuri R.M., Kimura M., Li W., Kim H.C., Lee H., Kiran M.D., Black W.C.t., Balagon M., Gelber R., Cho S.N., Brennan P.J., Vissa V. Population-based molecular epidemiology of leprosy in Cebu, Philippines. J. Clin. Microbiol. 2009, 47:2844-2854.
60. Salipante S.J., Horwitz M.S. Phylogenetic fate mapping. Proc. Natl. Acad. Sci. USA 2006, 103:5448-5453.
61. Scollard D.M., Adams L.B., Gillis T.P., Krahenbuhl J.L., Truman R.W., Williams D.L. The continuing challenges of leprosy. Clin. Microbiol. Rev. 2006, 19:338-381.
62. Shepard C.C. The experimental disease that follows the injection of human leprosy bacilli into footpads of mice. J. Exp. Med. 1960, 112:445-454.
63. Shepard C.C., McRae D.H. Mycobacterium leprae in mice. Minimal infectious dose, relationship between staining quality and infectivity, and effect of cortisone. J. Bacteriol. 1965, 89:365-372.
64. Shin Y.C., Lee H., Walsh G.P., Kim J.D., Cho S.N. Variable numbers of TTC repeats in Mycobacterium leprae DNA from leprosy patients and use in strain differentiation. J. Clin. Microbiol. 2000, 38:4535-4538.
65. Shinde V., Newton H., Sakamuri R.M., Reddy V., Jain S., Joseph A., Gillis T., Nath I., Norman G., Vissa V. VNTR typing of Mycobacterium leprae in South Indian leprosy patients. Lepr. Rev. 2009, 80:290-301.
66. Srisungnam S., Rudeeaneksin J., Lukebua A., Wattanapokayakit S., Pasadorn S., Mahotarn K., Ajincholapan, Sakamuri R.M., Kimura M., Brennan P.J., Phetsuksiri B., Vissa V. Molecular epidemiology of leprosy based on VNTR typing in Thailand. Lepr. Rev. 2009, 80:280-289.
67. Srisungngam S., Rudeeaneksin J., Wattanpokayakit S., Pasadorn S., Tragoolpua R., Suwanrit S., Sawanpanyalert P., Phetsuksiri B. Typing of Thai clinical isolates of Mycobacterium leprae and analysis of leprosy transmission by polymorphism of tandem repeats. Southeast Asian J. Trop. Med. Public Health 2007, 38:714-720.
68. Sterne J.A., Ponnighaus J.M., Fine P.E., Malema S.S. Geographic determinants of leprosy in Karonga District, Northern Malawi. Int. J. Epidemiol. 1995, 24:1211-1222.
69. Streisinger G., Okada Y., Emrich J., Newton J., Tsugita A., Terzaghi E., Inouye M. Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. Cold Spring Harb. Symp. Quant. Biol. 1966, 31:77-84.
70. Suzuki K., Udono T., Fujisawa M., Tanigawa K., Idani G., Ishii N. Infection during infancy and long incubation period of leprosy suggested in a case of a chimpanzee used for medical research. J. Clin. Microbiol. 2010, 48:3432-3434.
71. Tenover F.C., Arbeit R.D., Goering R.V., Mickelsen P.A., Murray B.E., Persing D.H., Swaminathan B. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 1995, 33:2233-2239.
72. Truman R. Leprosy in wild armadillos. Lepr. Rev. 2005, 76:198-208.
73. Truman R., Fine P.E. 'Environmental' sources of Mycobacterium leprae: issues and evidence. Lepr. Rev. 2010, 81:89-95.
74. Truman R., Fontes A.B., De Miranda A.B., Suffys P., Gillis T. Genotypic variation and stability of four variable-number tandem repeats and their suitability for discriminating strains of Mycobacterium leprae. J. Clin. Microbiol. 2004, 42:2558-2565.
75. Truman R.W., Singh P., Sharma R., Busso P., Rougemont J., Painz-Mondolfi A., Kapopoulou A., Brise S., Scollard S., Gillis T.P., Cole S.T. Probable zoonotic leprosy in the southern United States. N. Engl. J. Med. 2011, 364:1626-1633.
76. Welsh J., McClelland M. Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res. 1990, 18:7213-7218.
77. Weng X., Heiden J.V., Xing Y., Liu J., Vissa V. Transmission of leprosy in Qiubei County, Yunnan, China: Insights from an 8-year molecular epidemiology investigation. Infect Genet Evol. 2010, 11:363-374.
78. Weng X., Wang Z., Liu J., Kimura M., Black W.C.t., Brennan P.J., Li H., Vissa V.D. Identification and distribution of Mycobacterium leprae genotypes in a region of high leprosy prevalence in China: a 3-year molecular epidemiological study. J. Clin. Microbiol. 2007, 45:1728-1734.
79. Williams D.L., Gillis T.P., Portaels F. Geographically distinct isolates of Mycobacterium leprae exhibit no genotypic diversity by restriction fragment-length polymorphism analysis. Mol. Microbiol. 1990, 4:1653-1659.
80. Woods S.A., Cole S.T. A family of dispersed repeats in Mycobacterium leprae. Mol. Microbiol. 1990, 4:1745-1751.
81. Xing Y., Liu J., Sakamuri R.M., Wang Z., Wen Y., Vissa V., Weng X. VNTR typing studies of Mycobacterium leprae in China: assessment of methods and stability of markers during treatment. Lepr. Rev. 2009, 80:261-271.
82. Yamada N.A., Smith G.A., Castro A., Roques C.N., Boyer J.C., Farber R.A. Relative rates of insertion and deletion mutations in dinucleotide repeats of various lengths in mismatch repair proficient mouse and mismatch repair deficient human cells. Mutat. Res. 2002, 499:213-225.
83. Yang Z. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J. Mol. Evol. 1994, 39:306-314.
84. Young S.K., Ponnighaus J.M., Jain S., Lucas S., Suneetha S., Lockwood D.N., Young D.B., Fine P.E. Use of short tandem repeat sequences to study Mycobacterium leprae in leprosy patients in Malawi and India. PLoS Negl. Trop. Dis. 2008, 2:e214.
85. Young S.K., Taylor G.M., Jain S., Suneetha L.M., Suneetha S., Lockwood D.N., Young D.B. Microsatellite mapping of Mycobacterium leprae populations in infected humans. J. Clin. Microbiol. 2004, 42:4931-4936.
86. Zhang L., Budiawan T., Matsuoka M. Diversity of potential short tandem repeats in Mycobacterium leprae and application for molecular typing. J. Clin. Microbiol. 2005, 43:5221-5229.