What are the sources of Mycobacterium leprae?

by PatrĂ­cia Deps,

Full ProfessorDepartment of Social MedicinePostgraduate Program in Infectious Diseases, UFES. Brazil.

LetĂ­cia Pedrini,

Master's studentPostgraduate Program in Infectious Diseases, UFES. Brazil.

and Simon Collin.

Public Health England, London. United Kingdom.
11/01/2020

There is no doubt that a person affected by multibacillary Hansen’s disease who has not received specific treatment with multidrug therapy is the main, but not the only, source of infection of Mycobacterium leprae. However, there is incontestable evidence of zoonotic transmission of Hansen’s disease and the bacillus appears to survive in the environment.

Zoonoses are defined as ‘diseases or infections transmissible between vertebrate animals and humans’. In 2008, Truman reported that patients diagnosed with Hansen’s disease living in Texas, Louisiana and Mississippi, USA, reported no contact with other persons affected by the disease (1). Several years later, evidence was obtained that Hansen’s disease was a zoonosis by identifying a single strain of M leprae infecting Dasypus novemcinctus and people diagnosed with the disease (2).

The nine-banded armadillo (Dasypus novemcinctus) is a mammal of the order Xenarthra that in Brazil is known by variations on the Portuguese word for armadillo (tatu): tatu-verdadeiro, tatu-galinha, tatu-preto. Dasypus novemcinctus is the species of armadillo with the largest geographical distribution, extending from the south east of the United States to northern Argentina.

Among the other non-human environmental reservoirs of M. leprae are red squirrels in the British Isles, which have been found to be infected with the other known etiological agent of Hansen’s disease, M. lepromatosis (3). Although viable M. leprae have been found in water samples (4), soil from several countries (5), and plants (6), there is no consensus on environmental transmission of Hansen’s disease (7). Other than dated evidence of insects as potential vectors (8), viable M. leprae have been found in the gastrointestinal tract of triatoms (Rhodnius prolixus) (9), and within Entamoeba spp. which have phagocytosed the bacillus (10). It is possible that M. leprae uses Entamoeba spp. to survive in the environment and possibly infect other organisms.

A systematic review and meta-analysis by Deps et al. estimated that the prevalence of M. leprae in wild armadillos in Brazil was equivalent to 1 in 10 animals being infected, although without a uniform distribution of the infection throughout the country (11). Although the hunting of wild animals in Brazil is considered a crime (art. 29 of law 9.605/1998), the habit of capturing and consuming these animals is widespread and is influenced by socio-cultural factors.

Zoonotic transmission of Hansen’s disease is associated with contact, capture and consumption of armadillos (12). Whilst transmission from person to person is undoubtedly the main way of acquiring Hansen’s disease, the fraction of cases that could be attributed to zoonotic transmission is unknown. In Brazil, Hansen’s disease is not officially recognized as a zoonosis and avoidance of contact with or consumption of armadillos has not been included in guidelines. However, there is growing recognition that human health is strongly linked to animal and environmental health and a transdisciplinary One Health approach to Hansen’s disease is needed.

ReferĂªncias bibliogrĂ¡ficas

  1. Truman R. Armadillos as a Source of Infection for Leprosy. South Med J [Internet]. 2008 Jun;101(6):581–2. Available from: http://sma.org/southern-medical-journal/article/armadillos-as-a-source-of-infection-for-leprosy

  2. Truman RW, Singh P, Sharma R, Busso P, Rougemont J, Paniz-Mondolfi A, et al. Probable Zoonotic Leprosy in the Southern United States. N Engl J Med [Internet]. 2011 Apr 28;364(17):1626–33. Available from: http://www.nejm.org/doi/abs/10.1056/NEJMoa1010536

  3. Avanzi C, Del-Pozo J, Benjak A, Stevenson K, Simpson VR, Busso P, et al. Red squirrels in the British Isles are infected with leprosy bacilli. Science. 2016 Nov; 354(6313):744–7. Available from: https://doi.org/10.1126/science.aah3783 PMID: 27846605

  4. Mohanty PS, Naaz F, Katara D, Misba L, Kumar D, Dwivedi DK, et al. Viability of Mycobacterium leprae in the environment and its role in leprosy dissemination. Indian J Dermatol Venereol Leprol. 2016; 82(1):23–7. https://doi.org/10.4103/03786323.168935 PMID: 26728806

  5. Lavania M, Katoch K, Sachan P, Dubey A, Kapoor S, Kashyap M, et al. Detection of Mycobacterium leprae DNA from soil samples by PCR targeting RLEP sequences. J Commun Dis. 2006; 38(3):269– 73. PMID: 17373359

  6. Kazda J, Irgens LM, MĂ¼ller K. Isolation of non-cultivable acid-fast bacilli in sphagnum and moss vegetation by foot pad technique in mice. Int J Lepr Other Mycobact Dis. 1980; 48(1):1–6. PMID: 6988344

  7. Ploemacher T, Faber WR, Menke H, Rutten V, Pieters T. Reservoirs and transmission routes of leprosy; A systematic review. Franco-Paredes C, editor. PLoS Negl Trop Dis [Internet]. 2020 Apr 27;14(4):1–27. Available from: http://dx.doi.org/10.1371/journal.pntd.0008276

  8. Souza-Araujo HC de. PoderĂ¡ o carrapato transmitir a lepra? Mem Inst Oswaldo Cruz [Internet]. 1941;36(4):577–84. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0074-02761941000400002&lng=pt&tlng=pt

  9. Neumann A da S, Dias F de A, Ferreira J da S, Fontes ANB, Rosa PS, Macedo RE, et al. Experimental Infection of Rhodnius prolixus (Hemiptera, Triatominae) with Mycobacterium leprae Indicates Potential for Leprosy Transmission. Lanz-Mendoza H, editor. PLoS One [Internet]. 2016 May 20;11(5):e0156037. Available from: https://dx.plos.org/10.1371/journal.pone.0156037

  10. Lahiri R, Krahenbuhl JL. The role of free-living pathogenic amoeba in the transmission of leprosy: a proof of principle. Lepr Rev. 2008; 79(4):401–9. PMID: 19274986

  11. Deps P, Antunes JM, Santos AR, Collin SM. Prevalence of Mycobacterium leprae in armadillos in Brazil: A systematic review and meta-analysis. Franco-Paredes C, editor. PLoS Negl Trop Dis [Internet]. 2020 Mar 23;14(3):e0008127. Available from: https://dx.plos.org/10.1371/journal.pntd.0008127

  12. Deps P, Alves B, Gripp C, Aragao R, Guedes B, Filho J, et al. Contact with armadillos increases the risk of leprosy in Brazil: A case control study. Indian J Dermatol Venereol Leprol [Internet]. 2008;74(4):338. Available from: http://www.ijdvl.com/text.asp?2008/74/4/338/42897