Zoonotic risk of Hansen's disease from community contact with wild armadillos: A systematic review and meta‐analysis

Abstract

Understanding and quantifying the risk of Hansen's disease (HD) through zoonotic transmission of Mycobacterium leprae infection from wild armadillos is important because hunting, handling and consumption of these animals is widespread in communities where HD is endemic, posing a potential threat to the health of individuals and to HD elimination. We conducted a systematic review (PROSPERO CRD42019159891) of publications in MEDLINE, EMBASE, Global Health, Scopus, LILACS, Biblioteca Digital Brasileira de Teses e Dissertações, Catálogo de Teses e Dissertações de CAPES, and Biblioteca Virtual em Saúde up to 09/05/2020 using Mesh and text terms in English, Portuguese, Spanish and French. Random effects meta‐analyses were performed including of subgroups by endemicity and type of exposure. Seven of the nine included studies were case‐control, four from Brazil and three from the USA, comprising 1,124 cases and 2,023 controls in total. The other two studies, one from Brazil and one from Colombia, were cross‐sectional. The overall summary estimate (odds ratio, OR) for the relative odds of HD comparing people who had direct contact with armadillos and/or had eaten armadillo meat with those who had not was OR = 2.60 (95% CI 1.78–3.80, p < .001) with a predictive interval of OR = 1.10–6.17. Summary odds ratios for specific exposures were as follows: indirect contact, OR = 1.39 (95% CI 1.02, 1.89) (p = .04); eating, OR = 2.29 (95% CI 1.13, 4.66) (p = .02); hunting, OR = 2.54 (95% CI 1.21, 5.33) (p = .01). Most of the included studies had moderate risk of bias. Crude estimates were reduced by up to 24% when adjusted for confounders (where reported). Direct contact with wild armadillos was strongly associated with an increased risk of HD, whilst evidence for an increased risk of HD from indirect contact was weaker. The fraction of HD in endemic countries attributable to zoonotic transmission from armadillos remains unknown, but the precautionary principle needs to be adopted to protect public health.

Mycobacterium lepromatosis as a Second Agent of Hansen’s Disease

“…From a One Health perspective, HD in the United States is recognized as a zoonosis (Centers for Disease Control and Prevention, 2020), with genomic evidence linking M. leprae from armadillos in south eastern states with sporadic cases of HD (Truman et al, 2011;Sharma et al, 2015). In Brazil, where HD is endemic and hunting and consumption of armadillos is widespread, zoonotic transmission is generally regarded to be of little or no concern given the presumed predominance of human-to-human transmission, despite evidence that exposure to armadillos confers additional HD risk even in highly endemic areas (Deps et al, 2021). M. leprae has also been detected in environmental samples (Ploemacher et al, 2020), including in soil and water in areas endemic for HD in India (Mohanty et al, 2016;Singh et al, 2020), and from water sources in endemic areas in Brazil (Holanda et al, 2017).…”

Leprosy: what is new

“…One study suggests that there is an increased risk of HD in people who were living or working in armadillo inhabited areas, keeping armadillos as pets, and/or had eaten armadillo meat compared with those who had no form of armadillo contact. 13 PGL-1 is a M. leprae-specific cell wall component and a known biomarker for M. leprae infection in humans and armadillos. Although anti-PGL1 antibodies serologic evidence has very low sensitivity and low predictive value, it can be useful in leprosy exclusion.…”

“…The relationship between the consumption of armadillo meat and HD is not well established, although a significant relationship between capture, maintenance, and preparation of armadillo meat and HD has been identified. 13,17 The transmission mechanism between zoonotic reservoirs and susceptible individuals is unknown, but it is strongly suspected that direct contact poses a significant risk of leprosy development.…”

One Health and Hansen’s disease in Brazil

“…However, in the same group of patients, 68% reported direct contact (handling, butchering, or eating) with armadillos, compared with 48% of controls [24]. These data from Espírito Santo were combined in a recently published systematic review and meta-analysis with data from 2 other case-control studies, based in Ceará (2006) and Pará (2018), yielding a pooled odds ratio for Hansen's disease of 2.23 (95% confidence interval [CI] 1.73, 2.88) comparing people who had direct armadillo contact with those in the same communities who did not have direct contact [25]. In the 3 studies, direct contact was defined as hunting or eating (Ceará); hunting, eating, or handling (Espírito Santo); and hunting (Pará, where it was noted that all cases who hunted also ate armadillo meat).…”

“…This higher relative risk probably reflects the much lower background risk from person-toperson transmission in a non-endemic country. Other findings included an apparent doseresponse relationship, from indirect contact (1.4-fold odds) to hunting armadillos (2.5-fold odds) [25].…”