Zoonotic transmission of M. leprae in Brazil
One Health approach.
by Patrícia Duarte Deps.
Since 1971, American researchers have published that the armadillo reproduced Hansen's disease by experimentally inoculating Mycobacterium leprae. (1) In 1977, in the Southeast region of the USA, naturally infected armadillos of the species Dasypus novemcinctus were identified. (2) And soon after, although Hansen's disease is no longer endemic in the USA, autochthonous cases of persons diagnosed with the illness reported contact with armadillos, and no other risk factors for the disease were identified. (3)
In the 1980s, crucial information about Hansen's disease came from studies with armadillos, among them:
In the USA, armadillos may be naturally contaminated by M. leprae. (1)
The armadillos reproduce the disease, a systemic and neurocutaneous form, by experimental infection. (2)
In the USA, contact with armadillos is a risk factor for developing the disease. (3)
In the USA, Hansen's disease is a zoonosis. (4)
In Brazil, similar facts were reported. Studies published from 2002 to 2008 describe the presence of M. leprae DNA and anti-PGL-1 antibodies in armadillos of the species D. novemcintus in the state of Espírito Santo, endemic region for Hansen's disease in southeastern Brazil. (5-7) In the last two decades, more than 100 armadillos of the species D. novemcinctus and some other species were detected with natural infection by M. leprae in other states of Brazil. (8)
In 2006, an epidemiological survey conducted in the state of Espírito Santo was published. In this study, more than 50% of the 506 people affected by Hansen's disease did not know the source of bacilli, i.e. they reported having had no known contact with any sick person. (9)
In another case control study it was found that 68% of people affected by the infection, as well as 48% of controls, reported direct contact with armadillos. (10) In addition, three other case-control studies were conducted in Brazil and analyzed in conjunction with three other US studies. The odds ratio found was a relative risk of 2.60 for Hansen's disease in people who had direct contact (hunting, cleaning and/or eating) with armadillos, compared to those who did not. The relative risk for indirect contact was 1.39. (11)
What can we conclude from these surveys?
Despite many unanswered questions, we can consider that Hansen's disease is a zoonosis also in Brazil.
Zoonosis is an infectious disease in which the same etiological agent causes disease in humans and vertebrate animals. If Hansen's disease is a zoonosis in the USA, there is no reason to think that it is not in Brazil. Although the environment is not the same, we refer to hominids of the species Homo sapiens sapiens, to armadillos that are of the same species Dasypus novemcinctus, and to the microorganism that is Mycobacterium leprae. The same strain of M. leprae was found in armadillos and human beings affected by Hansen's disease in the USA. (12,13)
In the USA, in a person diagnosed with Hansen's disease who does not report living with another sick person, direct or indirect contact with an armadillo becomes the most relevant risk factor. (13)
In Brazil, a person diagnosed with Hansen's disease reported having had contact with someone sick in 44% of cases, (9) and in 68% of cases direct or indirect contact with armadillos was also reported. (10)
Thus, Hansen's disease in Brazil can have a zoonotic transmission. Possibly, the Hansen's bacillus is spread in the environment by man and armadillo, and both acquire the infection from each other and the environment (Figure 1).
Figure 1. Zoonotic transmission of Mycobacterium leprae in the Americas.
Vertebrate animal - Human – Environment (microorganism).
The three pillars of zoonosis need to be characterized. Currently, there is no doubt that man, the armadillo and M. leprae are related, however, their origin is unknown. The armadillos belong to the Superorder of placental mammals called Xenarthra (Xenarthra) and have inhabited the center of North America, Central and South America for 60 million years. (14) Homo sapiens sapiens has inhabited the Americas for at least 15-20,000 years. (15) Possibly the last to arrive in the American continent was the pathogenic microorganism, Mycobacterium leprae. The strains of M. leprae have spread to Asia, Europe, Africa and the Americas. (12) The first case of Hansen's disease in Brazil was identified in the state of Rio de Janeiro in mid-1600. According to historians, the disease came to Brazil during the European colonization process, but there was still a small contribution from Africans who were trafficked to Brazil. (16)
Therefore, it is reasonable to theorize that M. leprae was brought from Europe to Brazil and that these microorganisms contaminated soil, water and vegetation and, consequently, infected the armadillos. The armadillos are animals very susceptible to infection, harboring and multiplying the pathogen in their bodies and becoming an environmental source of the bacillus for humans. Eventually, when man comes into direct contact with the animal, they contaminate the environment.
The participation of armadillos in the endemic in Brazil is uncertain. However, assuming that One Health approach deal with the protection of human and animal health through ecological balance and environmental preservation, it is not possible to disregard this source of bacilli for humans and the environment.
Informing health professionals and the population about the risk of contamination by M. leprae through contact with armadillos should be the responsibility of the scientific community and authorities of each area involved.
Storrs EE. The nine-banded armadillo: a model for leprosy and other biomedical research. Int J Lepr Other Mycobact Dis ;39:703-14. 1971;
Kirchheimer WF. Occurrence of Mycobacterium leprae in nature. Leprosy in India. 1977;49:44.
Bruce S, Schroeder TL, Kenneth E, Howard R, Willians T, Wolf JE. Armadillo exposure and Hansen’s disease: an epidemiologic survey in southern Texas. 2000;43:223–8.
Walsh GP, Meyers WM, Binford CH, Gerome PJ, Wolf RH, Leininger JR. Leprosy - a zoonosis. Lepr Rev. 1981;52:77–83.
Deps PD, Antunes JM, Faria C, Buhrer-Sekula S, Camargo ZP, Opromola DV, et al. Research regarding anti-PGL-I antibodies by ELISA in wild armadillos from Brazil. Rev Soc Bras Med Trop. 2008; 41 Suppl 2(SUPPL. 2):73–6. Epub 2008/01/01.
Deps PD, Antunes JM, Tomimori-Yamashita J. Detection of Mycobacterium leprae infection in wild nine-banded armadillos (Dasypus novemcinctus) using the rapid ML Flow test. Rev Soc Bras Med Trop. 2007; 40(1):86–7. Epub 2007/05/09.
Deps PD, Santos AR, Yamashita-Tomimori J. Detection of Mycobacterium leprae DNA by PCR in blood sample from nine-banded armadillo: preliminary results. Int J Lepr Other Mycobact Dis. 2002; 70(1):34–5.
Deps, P., J. M. Antunes, A. R. Santos and S. M. Collin, 2020: Prevalence of Mycobacterium leprae in armadillos in Brazil: A systematic review and meta-analysis. PLoS Negl.Trop. Dis., 14, e0008127.
Deps, P. D., B. V. Guedes, J. Bucker Filho, M. K. Andreatta, R. S. Marcari and L. C. Rodrigues, 2006: Characteristics of known leprosy contact in a high endemic area in Brazil. Lepr. Rev., 77, 34-40.
Deps, P. D., B. L. Alves, C. G. Gripp, R. L. Aragao, B. Guedes, J. B. Filho, M. K. Andreatta, R. S. Marcari, I. Prates and L. C. Rodrigues, 2008: Contact with armadillos increases the risk of leprosy in Brazil: a case control study. Indian J. Dermatol. Venereol. Leprol., 74, 338-342.
Deps P, Antunes JMA, Collin S. Zoonotic risk of Hansen’s disease from community contact with wild armadillos: a systematic review and meta-analysis. Zoonosis and Public Health. In press.
Monot M, Honore N, Garnier T, Araoz R, Coppee JY, Lacroix C, et al. On the origin of leprosy. Science. 2005; 308(5724):1040–2. Epub 2005/05/17. https://doi.org/10.1126/science/1109759.
Sharma R, Singh P, Loughry WJ, Lockhart JM, Inman WB, Duthie MS, et al. Zoonotic leprosy in the southeastern United States. Emerg Infect Dis. 2015;21.
Vizcaíno FS, Loughry WJ. Xenarthran biology: past, present, and future. In: Vizcaíno, SF and Loughry WF, editors. The biology of the xenarthra. Gainesville University Press of 2008. P.1-7.
DNA study links indigenous Brazilians to Polynesians. Nature. http://www.nature.com/news/dna-study-links-indigenous-brazilians-to-polynesians-1.12710.
Yamanouchi, A. A.; Caron, C. R.; Shiwaku, D. T. et al. Hanseníase e sociedade: um problema sempre atual. Anais Brasileiros de Dermatologia. 1993;68(6):396–404.