Environmental sources of Mycobacterium leprae

by Patrícia D. Deps,

Department of Social Medicine, Post-Graduate Program in Infectious Diseases, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil.

João Marcelo Antunes,

Federal University of Rural of Semi-Árido, Hospital Veterinário Jerônimo Dix-Huit Rosado Maia, Mossoró, Rio Grande do Norte, Brazil

and Simon M. Collin.

Public Health England, London, United Kingdom.

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.

Mammals

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.

Fig 1. Relative risk of Hansen's disease (odds ratio, OR) comparing groups exposed to wild armadillos with groups not exposed.
Academic Collaborators

Laysa da Silva Madeira e

Thiago Capini Santos

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