Reports

On the Origin of Leprosy

Marc Monot,^1* Nadine Honoré,^1* Thierry Garnier,¹ Romulo Araoz,¹ Jean-Yves Coppée,² Céline Lacroix,² Samba Sow,³ John S. Spencer,⁴ Richard W. Truman,⁵ Diana L. Williams,⁵ Robert Gelber,⁶ Marcos Virmond,⁷ Béatrice Flageul,⁸ Sang-Nae Cho,⁹ Baohong Ji,¹⁰ Alberto Paniz-Mondolfi,¹¹ Jacinto Convit,¹¹ Saroj Young,¹² Paul E. Fine,¹² Voahangy Rasolofo,¹³ Patrick J. Brennan,⁴ Stewart T. Cole¹

Leprosy, a chronic human disease with potentially debilitating neurological consequences, results from infection with Mycobacterium leprae. This unculturable pathogen has undergone extensive reductive evolution, with half of its genome now occupied by pseudogenes. Using comparative genomics, we demonstrated that all extant cases of leprosy are attributable to a single clone whose dissemination worldwide can be retraced from analysis of very rare single-nucleotide polymorphisms. The disease seems to have originated in Eastern Africa or the Near East and spread with successive human migrations. Europeans or North Africans introduced leprosy into West Africa and the Americas within the past 500 years.

¹ Unité de Génétique Moléculaire Bactérienne, Institut Pasteur, Paris, France.
² PF2, Génopole, Institut Pasteur, Paris, France.
³ Centre National d'Appui à la lutte Contre la Maladie, Bamako, Mali.
⁴ Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado 80523–1682, USA.
⁵ National Hansen's Disease Program, DHHS/HRSA/BPHC, Lousiana State University, Baton Rouge, Lousiana 70894, USA.
⁶ Leonard Wood Memorial Center for Leprosy Research, Cebu, Philippines.
⁷ Instituto Lauro de Souza Lima, Bauru, São Paulo, Brazil.
⁸ Hôpital Saint-Louis, Paris, France.
⁹ Yonsei University College of Medicine, Seoul, Republic of Korea.
¹⁰ Bactériologie-Hygiène, Faculté de Médecine Pitié-Salpêtrière, Paris, France.
¹¹ Instituto de Biomedicina, Caracas, Venezuela.
¹² London School of Hygiene and Tropical Medicine, London, UK.
¹³ Institut Pasteur de Madagascar, Antananarivo, Madagascar.

^* These authors contributed equally to this work.

To whom correspondence should be addressed: E-mail: stcole{at}pasteur.fr

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Comparative Sequence Analysis of Mycobacterium leprae and the New Leprosy-Causing Mycobacterium lepromatosis.

X. Y. Han, K. C. Sizer, E. J. Thompson, J. Kabanja, J. Li, P. Hu, L. Gomez-Valero, and F. J. Silva (2009)
J. Bacteriol. 191, 6067-6074
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Population-Based Molecular Epidemiology of Leprosy in Cebu, Philippines.

R. M. Sakamuri, M. Kimura, W. Li, H.-C. Kim, H. Lee, M. D. Kiran, W. C. Black IV, M. Balagon, R. Gelber, S.-N. Cho, et al. (2009)
J. Clin. Microbiol. 47, 2844-2854
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Rapid Variable-Number Tandem-Repeat Genotyping for Mycobacterium leprae Clinical Specimens.

M. Kimura, R. M. Sakamuri, N. A. Groathouse, B. L. Rivoire, D. Gingrich, S. Krueger-Koplin, S.-N. Cho, P. J. Brennan, and V. Vissa (2009)
J. Clin. Microbiol. 47, 1757-1766
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Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae.

M. Brochet, C. Rusniok, E. Couve, S. Dramsi, C. Poyart, P. Trieu-Cuot, F. Kunst, and P. Glaser (2008)
PNAS 105, 15961-15966
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Are Variable-Number Tandem Repeats Appropriate for Genotyping Mycobacterium leprae?.

M. Monot, N. Honore, C. Baliere, B. Ji, S. Sow, P. J. Brennan, and S. T. Cole (2008)
J. Clin. Microbiol. 46, 2291-2297
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Case-control Study of Armadillo Contact and Hansen's Disease.

B. M. Clark, C. K. Murray, L. L. Horvath, G. A. Deye, M. S. Rasnake, and R. N. Longfield (2008)
Am J Trop Med Hyg 78, 962-967
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The Carriage Population of Staphylococcus aureus from Mali Is Composed of a Combination of Pandemic Clones and the Divergent Panton-Valentine Leukocidin-Positive Genotype ST152.

R. Ruimy, A. Maiga, L. Armand-Lefevre, I. Maiga, A. Diallo, A. K. Koumare, K. Ouattara, S. Soumare, K. Gaillard, J.-C. Lucet, et al. (2008)
J. Bacteriol. 190, 3962-3968
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Genomics of Actinobacteria: Tracing the Evolutionary History of an Ancient Phylum.

M. Ventura, C. Canchaya, A. Tauch, G. Chandra, G. F. Fitzgerald, K. F. Chater, and D. van Sinderen (2007)
Microbiol. Mol. Biol. Rev. 71, 495-548
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Microevolution and Patterns of Dissemination of the JP2 Clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans.

D. Haubek, K. Poulsen, and M. Kilian (2007)
Infect. Immun. 75, 3080-3088
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Identification and Distribution of Mycobacterium leprae Genotypes in a Region of High Leprosy Prevalence in China: a 3-Year Molecular Epidemiological Study.

X. Weng, Z. Wang, J. Liu, M. Kimura, W. C. Black IV, P. J. Brennan, H. Li, and V. D. Vissa (2007)
J. Clin. Microbiol. 45, 1728-1734
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The Continuing Challenges of Leprosy.

D. M. Scollard, L. B. Adams, T. P. Gillis, J. L. Krahenbuhl, R. W. Truman, and D. L. Williams (2006)
Clin. Microbiol. Rev. 19, 338-381
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Isothermal Amplification and Molecular Typing of the Obligate Intracellular Pathogen Mycobacterium leprae Isolated from Tissues of Unknown Origins.

N. A. Groathouse, S. E. Brown, D. L. Knudson, P. J. Brennan, and R. A. Slayden (2006)
J. Clin. Microbiol. 44, 1502-1508
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Variable host-pathogen compatibility in Mycobacterium tuberculosis.

S. Gagneux, K. DeRiemer, T. Van, M. Kato-Maeda, B. C. de Jong, S. Narayanan, M. Nicol, S. Niemann, K. Kremer, M. C. Gutierrez, et al. (2006)
PNAS 103, 2869-2873
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Minerva.

(2005)
BMJ 331, E374
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Worldwide Clonal Migration of Leprosy.

(2005)
Journal Watch Infectious Diseases 2005, 8
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Minerva.

(2005)
BMJ 330, 1218
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