Evidence of zoonotic leprosy in Pará, Brazilian Amazon, and risks associated with human contact or consumption of armadillos

Abstract

Mycobacterium leprae (M. leprae) is a human pathogen and the causative agent for leprosy, a chronic disease characterized by lesions of the skin and peripheral nerve damage. Zoonotic transmission of M. leprae to humans by nine-banded armadillos (Dasypus novemcinctus) has been shown to occur in the southern United States, mainly in Texas, Louisiana, and Florida. Nine-banded armadillos are also common in South America, and residents living in some areas in Brazil hunt and kill armadillos as a dietary source of protein. This study examines the extent of M. leprae infection in wild armadillos and whether these New World mammals may be a natural reservoir for leprosy transmission in Brazil, similar to the situation in the southern states of the U.S. The presence of the M. leprae-specific repetitive sequence RLEP was detected by PCR amplification in purified DNA extracted from armadillo spleen and liver tissue samples. A positive RLEP signal was confirmed in 62% of the armadillos (10/16), indicating high rates of infection with M. leprae. Immunohistochemistry of sections of infected armadillo spleens revealed mycobacterial DNA and cell wall constituents in situ detected by SYBR Gold and auramine/rhodamine staining techniques, respectively. The M. leprae-specific antigen, phenolic glycolipid I (PGL-I) was detected in spleen sections using a rabbit polyclonal antibody specific for PGL-I. Anti-PGL-I titers were assessed by ELISA in sera from 146 inhabitants of Belterra, a hyperendemic city located in western Pará state in Brazil. A positive anti-PGL-I titer is a known biomarker for M. leprae infection in both humans and armadillos. Individuals who consumed armadillo meat most frequently (more than once per month) showed a significantly higher anti-PGL-I titer than those who did not eat or ate less frequently than once per month. Armadillos infected with M. leprae represent a potential environmental reservoir. Consequently, people who hunt, kill, or process or eat armadillo meat are at a higher risk for infection with M. leprae from these animals.

Prevalence of Mycobacterium leprae in armadillos in Brazil: A systematic review and meta-analysis

“…Five of the full text articles assessed for eligibility were theses or dissertations [7,[23][24][25]28]. The full PCR results from two of these had been published in peer-reviewed papers that we included for data extraction: Pedrini 2006 thesis [24] in Pedrini et al 2010 [9]; Portela 2015 dissertation [25] in da Silva et al 2018 [3]. PCR results from the Deps 2003 thesis [23] were published as preliminary findings in Deps et al 2002 [6]; PCR results from the Antunes 2007 dissertation [7] and de Souza dissertation [28] had not yet been published.…”

“…The first report of natural infection of M. leprae in wild armadillos in Brazil was a preliminary finding in 2002 based on PCR analysis of blood samples from 14 nine-banded armadillos (Dasypus novemcinctus) from the south-eastern state of Espírito Santo [6]. A later study confirmed these findings in Espírito Santo [7], and M. leprae was subsequently reported in wild armadillos from the northern states of Ceará [8] and Pará [3]. Conversely, studies in São Paulo and Mato Grosso do Sul [9] and Amazonas [10] found no M. leprae in wild armadillos.…”

“…Understanding the prevalence of M. leprae infection in armadillos is of public health importance because of epidemiological evidence from Brazil and other countries of an association between contact with armadillos and the development of Hansen's Disease (leprosy) in people [1][2][3][4][5]. The first report of natural infection of M. leprae in wild armadillos in Brazil was a preliminary finding in 2002 based on PCR analysis of blood samples from 14 nine-banded armadillos (Dasypus novemcinctus) from the south-eastern state of Espírito Santo [6].…”

Cutaneous Mycobacterial Infections

“…Zoonotic transmission from armadillos acting as reservoirs of infection has been confirmed for autochthonous southeast United States cases (51,52). Armadillos may also play a role in the transmission of leprosy in some areas in Colombia (55) and in Brazil (56). In some of the British Isles, red squirrels may develop leprosy-like lesions due to either M. leprae or Mycobacterium lepromatosis (53).…”

“…The precise mode of transmission of leprosy remains uncertain but probably involves human-to-human contact through respiratory droplets (29,30,(45)(46)(47) or through blood transfusion (48). Ecological data suggest that environmental factors, such as trauma or skin breaks during soil and water exposures, insect vectors, free-living amoebas, and animal reservoirs (e.g., armadillos, squirrels, felines, or other animals), influence leprosy transmission (39,47,(49)(50)(51)(52)(53)(54)(55)(56)(57)(58)(59)(60)(61)(62)(63). Zoonotic transmission from armadillos acting as reservoirs of infection has been confirmed for autochthonous southeast United States cases (51,52).…”