Environmental sources of Mycobacterium leprae
by Patrícia D. Deps,
João Marcelo Antunes,
and Simon M. Collin.
Doubts as to whether Hansen’s disease is transmitted exclusively from person to person are very old. At the Second International Leprosy Congress in 1909, it was suggested that M. leprae could exist in soil and in animals and be transmitted to humans. Hansen’s disease is considered a zoonosis in the United States,1 with sporadic cases occurring from direct contact with wild armadillos,2,3 or from work in areas inhabited by armadillos.4 Environmental samples have shown that M. leprae and M. lepromatosis can persist in soil and water in animal habitats and in Hansen’s disease-endemic populated areas.5
Soil, water and M. leprae with other microorganisms
Viable M. leprae and M. lepromatosis can be found in the environment, particularly in soil and water from places where the disease is endemic,6-8 but the importance of environmental contamination in the transmission of the disease is not yet well established, and evidence of a higher prevalence of Hansen’s disease in individuals who used water contaminated with M. leprae is probably the reverse-causation.9
The coexistence of M. leprae with Acanthamoeba spp., free-living protozoa, has been identified, suggesting sustained survival of the Hansen’s disease-causing bacillus in the environment.10 The importance of M. leprae infected protozoa in Hansen’s disease transmission is unknown.11,12
Amphibians and arthropods
Since the mid-20th century, several studies have been conducted in search of the answer about other viable forms of transmission of M. leprae, specifically ticks, bed bugs, fleas, lice, and mosquitoes.13-16
Acid-fast bacilli were detected in Aedes aegypti and Culex fatigans shortly after biting people affected by Hansen’s disease, but the bacterial species was not identified.17 M. leprae DNA was found in hematophagous bedbugs (Rhodnius prolixus) by the PCR technique,18 and tick species (Amblyomma sculptum) and tick cell lines Ixodes scapularis were experimentally infected with M. leprae.19 Thus, there is evidence that arthropods appear to have the potential to carry M. leprae, but there is as yet no evidence of transmission to humans.
Studies have shown the presence of M. leprae in some mammal species such as buffalo,20 chimpanzees,21 and mangabe monkeys,22 and M. lepromatosis in red squirrels.23 Armadillos have emerged as the most important animals for the study of the disease,24 because they are susceptible to laboratory and natural M. leprae infection and are an ideal animal model for reproducing Hansen’s disease.25 Armadillos of the species Dasypus novemcinctus and Euphractus sexcinctus, but also other species, are susceptible to M. leprae, and are therefore considered a potential source of infection for humans.26,27
Consequently, it was proposed that armadillo species could serve as reservoirs of M. leprae and act as zoonotic transmitters of the disease. Evidence supporting an increased risk of Hansen’s disease through contact with infected wild armadillos or M. leprae carriers comes from a number of studies conducted in Brazil and the USA.
Five studies were based in Brazil, one in the state of Paraná,28 two in Espírito Santo,29,30 one in Ceará,31 and one in Pará.32 All except the Pará study were case-control studies recruiting persons affected by Hansen’s disease from outpatient clinics, although the Deps et al. 2003 study also recruited patients who previously had Hansen’s disease from a "colony" hospital. Controls were selected from patients who attended the same clinics for other reasons. The Pará study was based on a research visit to two villages, with 7 cases (3 previously diagnosed, 4 diagnosed by the study team) among a sample of 146 people.
The three US studies had a case-control design, with cases identified at an outpatient facility of the Texas Center for Infectious Diseases in San Antonio,33 reported last year to the state health department or the Public Health Service Hospital in Carville, Louisiana,34 and attending an outpatient facility of the Los Angeles County - University of Southern California Medical Center.35
A meta-analysis based on these studies shows that people who have direct contact with and/or eat armadillo meat are more than twice as likely to develop Hansen’s disease as people who do not eat or have contact with armadillo (Figure 1).
In Brazil, where hunting and consumption of armadillos is a common practice is illegal,36 the fraction of Hansen’s disease in the population attributable to contact or consumption of armadillos will depend on the magnitude of the risk, the type and frequency of contact and consumption, and how common these practices are in the communities, along with the contribution of other transmission routes (human to human) of M. leprae and the immune susceptibility of individuals. In countries with low Hansen’s disease incidence and in countries seeking to eliminate Hansen’s disease, zoonotic and other environmental reservoirs of infection may be important. In endemic countries, recommendations concerning zoonotic reservoirs need to be incorporated into the official Hansen’s disease control guidelines.
Laysa da Silva Madeira e
Thiago Capini Santos
Transmission | Hansen’s Disease (Leprosy) | CDC. (2019). Available at: https://www.cdc.gov/leprosy/transmission/index.html. (Accessed: 12th May 2020)
Lumpkin, L. R. 3rd, Cox, G. F. & Wolf, J. E. J. Leprosy in five armadillo handlers. J Am Acad Dermatol 9, 899–903 (1983).
Domozych, R., Kim, E., Hart, S. & Greenwald, J. Increasing incidence of leprosy and transmission from armadillos in Central Florida: A case series. JAAD Case Rep 2, 189–192 (2016).
Mohan, S. & Fairley, J. K. A Challenging Case of Domestically Acquired Leprosy in the Southern United States. Open Forum Infect Dis 7, (2020).
Ploemacher, T., Faber, W. R., Menke, H., Rutten, V. & Pieters, T. Reservoirs and transmission routes of leprosy; A systematic review. PLoS Negl Trop Dis 14, e0008276 (2020).
Turankar, R. P. et al. Association of non-tuberculous mycobacteria with Mycobacterium leprae in environment of leprosy endemic regions in India. Infect. Genet. Evol. 72, 191–198 (2019).
Lavania, M. et al. Detection of viable Mycobacterium leprae in soil samples: insights into possible sources of transmission of leprosy. Infect. Genet. Evol. 8, 627–631 (2008).
Mohanty, P. S. et al. Viability of Mycobacterium leprae in the environment and its role in leprosy dissemination. Indian J Dermatol Venereol Leprol 82, 23–27 (2016).
Matsuoka, M., Izumi, S., Budiawan, T., Nakata, N. & Saeki, K. Mycobacterium leprae DNA in daily using water as a possible source of leprosy infection. Indian J Lepr 71, 61–67 (1999).
Turankar, R. P. et al. Survival of Mycobacterium leprae and association with Acanthamoeba from environmental samples in the inhabitant areas of active leprosy cases: A cross sectional study from endemic pockets of Purulia, West Bengal. Infect. Genet. Evol. 72, 199–204 (2019).
Lahiri, R. & Krahenbuhl, J. L. The role of free-living pathogenic amoeba in the transmission of leprosy: a proof of principle. Lepr Rev 79, 401–409 (2008).
Wheat, W. H. et al. Long-term survival and virulence of Mycobacterium leprae in amoebal cysts. PLoS Negl Trop Dis 8, e3405 (2014).
Souza-Araujo, H. C. de & Souza-Araujo, H. C. de. Poderá o carrapato transmitir a lepra? Memórias do Instituto Oswaldo Cruz 36, 577–584 (1941).
Narayanan, E., Manja, K. S., Bedi, B. M., Kirchheimer, W. F. & Balasubrahmanyan, M. Arthropod feeding experiments in lepromatous leprosy. Lepr Rev 43, 188–193 (1972).
Geater, J. G. The fly as potential vector in the transmission of leprosy. Lepr Rev 46, 279–286 (1975).
Blake, L. A., West, B. C., Lary, C. H. & Todd, J. R. Environmental nonhuman sources of leprosy. Rev. Infect. Dis. 9, 562–577 (1987).
Bona, S. H., da Silva, A. C. L. & da Costa, R. J. Bacilos álcool-ácido resistentes no Culex fatigans. An Bras Dermatol 60, (1985).
Neumann, A. da S. et al. Experimental Infection of Rhodnius prolixus (Hemiptera, Triatominae) with Mycobacterium leprae Indicates Potential for Leprosy Transmission. PLoS ONE 11, e0156037 (2016).
Ferreira, J. da S. et al. Ticks as potential vectors of Mycobacterium leprae: Use of tick cell lines to culture the bacilli and generate transgenic strains. PLoS Negl Trop Dis 12, (2018).
Lobel, L. W. M. Lepra bubalorum. Int. J. Lepr. 4, 79–96 (1936).
Donham, K. J. & Leininger, J. R. Spontaneous leprosy-like disease in a chimpanzee. J. Infect. Dis. 136, 132–136 (1977).
Walsh, G. P. et al. Leprosy--a zoonosis. Lepr Rev 52 Suppl 1, 77–83 (1981).
Avanzi, C. et al. Red squirrels in the British Isles are infected with leprosy bacilli. Science 354, 744–747 (2016).
Truman, R. W., Morales, M. J., Shannon, E. J. & Hastings, R. C. Evaluation of monitoring antibodies to PGL-I in armadillos experimentally infected with M. leprae. Int J Lepr Other Mycobact Dis 54, 556–559 (1986).
Oliveira, I. V. P. de M., Deps, P. D. & Antunes, J. M. A. de P. Armadillos and leprosy: from infection to biological model. Rev Inst Med Trop Sao Paulo 61,
Truman, R. W. et al. Probable zoonotic leprosy in the southern United States. N Engl J Med 364, 1626–1633 (2011).
Deps, P., Antunes, J. M., Santos, A. R. & Collin, S. M. Prevalence of Mycobacterium leprae in armadillos in Brazil: A systematic review and meta-analysis. PLoS Negl Trop Dis 14, (2020).
Deps, P. D. et al. Contact with armadillos increases the risk of leprosy in Brazil: a case control study. Indian J Dermatol Venereol Leprol 74, 338–342 (2008).
Thomas, D. A., Mines, J. S., Thomas, D. C., Mack, T. M. & Rea, T. H. Armadillo exposure among Mexican-born patients with lepromatous leprosy. J Infect Dis 156, 990–992 (1987).
Schmitt, J. V. et al. Armadillo meat intake was not associated with leprosy in a case control study, Curitiba (Brazil). Mem Inst Oswaldo Cruz 105, 857–62 (2010).
Deps, P. D. et al. Aspectos epidemiológicos da transmissão da hanseníase em relação a exposição ao tatu. Hansenologia Internationalis (Online) 28, 138–144 (2003).
Kerr-Pontes, L. R. S. et al. Socioeconomic, environmental, and behavioural risk factors for leprosy in North-east Brazil: results of a case-control study. Int J Epidemiol 35, 994–1000 (2006).
da Silva, M. B. et al. Evidence of zoonotic leprosy in Para, Brazilian Amazon, and risks associated with human contact or consumption of armadillos. PLoS Negl Trop Dis 12, e0006532 (2018).
Clark, B. M. et al. Case-control study of armadillo contact and Hansen’s disease. The American journal of tropical medicine and hygiene 78, 962–7 (2008).
Filice, G. A., Greenberg, R. N. & Fraser, D. W. Lack of observed association between armadillo contact and leprosy in humans. The American journal of tropical medicine and hygiene 26, 137–9 (1977).
Kerr, L. et al. Human-armadillo interaction in Ceara, Brazil: Potential for transmission of Mycobacterium leprae. Acta Trop 152, 74–79 (2015).