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Vol. 22. Num. 5.September - October 2018
Pages 359-448
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Vol. 22. Num. 5.September - October 2018
Pages 359-448
Letter to the editor
DOI: 10.1016/j.bjid.2018.09.003
Open Access
Molecular detection of Mycobacterium leprae by Polymerase Chain Reaction in captive and free-ranging wild animals
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Fernanda H. Maruyama, Thais O. Morgado, Richard C. Pacheco, Luciano Nakazato, Valeria Dutra
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valeriadutra.dutra@gmail.com

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Universidade Federal do Mato Grosso, Pós-Graduação em Ciências Veterinárias, Departamento de Veterinária, Mato Grosso, MT, Brazil
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Table 1. Epidemiological data and M. leprae PCR test of the animals identified in Mato Grosso – Brazil.
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Leprosy, a disease neglected in many countries, is endemic in Brazil. With a wide diversity of fauna distributed in three biomes (Amazon Forest, Cerrado and Pantanal), the state of Mato Grosso (MT) in the Central-West Region has the highest prevalence of human cases: 7.75 per 10,000 inhabitants.1 Despite the scarcity of data in the literature on wild animals naturally infected with Mycobacterium leprae, the possibility of transmission to humans cannot be ruled out. Armadillos, red squirrels, and non-human primates are important natural reservoirs of M. leprae reported in the literature, becoming possible sources of bacillary dissemination making it difficult to interrupt the leprosy transmission chain.2 As data on natural infections are scarce, it is difficult to understand the role of wild animals in transmission of the disease. Therefore, we used PCR to detect the genetic material of M. leprae in nasal swabs of wild animals.

Nasal swabs were collected from 69 captive and free wild animals from the MT and Pantanal regions of Brazil, independent of clinical signs, and sent to the Laboratory of Microbiology and Molecular Biology, according to “Sistema de Autorização e Informação em Biodiversidade” (SISBIO), an authorization and information system for biodiversity (nos. 40617-1 and 42303). The samples were submitted for extraction of genetic material according to the phenol/chloroform method. PCR was performed according to Woods and Cole.3 The PCR product was purified using a GFX™ PCR DNA and Gel Band Purification kit (GE Healthcare, Piscataway, NJ, USA) and sequenced using an ABI-PRISM 3500 Genetic Analyzer (Life Technologies Corporation, USA). The sequences were deposited in GenBank and compared using the BLAST program (http://www.ncbi.nlm.nih.gov/blast/Blast.cgi). Of the 69 samples (Table 1), six (8.69%) wild-type free and captive animals tested positive for M. leprae by PCR, including one margay (Leopardus wiedii), two lowland tapirs (Tapirus terrestris), two capuchin monkeys (Sapajus apella), and one owl monkey (Aotus trivirgatus). The detection in four different species of wild animals shows the ability of this bacillus to be carried in different hosts. In addition, two animals were from the zoo, that could have acquired M. leprae due to close contact to humans or environmental contamination. However, in literature the mechanism of transmission is not yet fully understood.4

Table 1.

Epidemiological data and M. leprae PCR test of the animals identified in Mato Grosso – Brazil.

ID  Free-ranging  City  Species  Scientific name  PCR 
m962/16  Yes  Jangada  Jaguarundi  Puma yagouaroundi  Negative 
m1016/16  Yes  Marcelândia  Jaguar  Panthera onca  Negative 
m1102/16  No  Zooa  Cougar  Puma concolor  Negative 
m1122/16  No  Zoo  Coati  Nasua nasua  Negative 
m1162/16  Yes  Cuiabá  Guinea pig  Cavia porcellus  Negative 
m1226/16  Yes  Barra do Bugres  Ocelot  Leopardus pardalis  Negative 
m1285/16  Yes  NAb  Jaguarundi  Puma yagouaroundi  Negative 
m1294/16  Yes  Várzea Grande  Capybara  Hydrochoerus hydrochaeris  Negative 
m1335/16  No  Zoo  Giant anteater  Myrmecophaga tridactyla  Negative 
m1336/16  Yes  Rosário Oeste  Giant anteater  Myrmecophaga tridactyla  Negative 
m1364/16  Yes  Cuiabá  Collared anteaters  Myrmecophaga tetradactyla  Negative 
m1485/16  Yes  Santo Antônio do Leverger  Otter  Lontra longicaudis  Negative 
m1491/16  Yes  NA  White-eared opossum  Didelphis albiventris  Negative 
m1529/16  No  Zoo  Agouti  Dasyprocta Aguti  Negative 
m1787/17  Yes  NA  Owl monkey  Aoutus trivirgatus
 
Positive Genbank MF975704 
m1790/16  Yes  Tangará da Serra  Giant anteater  Myrmecophaga tridactyla  Negative 
m1795/16  No  Zoo  Coati  Nasua nasua  Negative 
m1796/16  No  Zoo  Agouti  Dasyprocta aguti  Negative 
m1862/16  Yes  Várzea Grande  Collared anteaters  Myrmecophaga tetradactyla  Negative 
m11/17  Yes  Cuiabá  Capuchin monkey  Sapajus apella  Positive Genbank MF975703 
m74/17  No  Zoo  Cougar  Puma concolor  Negative 
m153/17  Yes  Cuiabá  White-eared opossum  Didelphis albiventris  Negative 
m234/17  No  Zoo  Cougar  Puma concolor  Negative 
m235/17  Yes  Cuiabá  Sagui  Callithrix sp.  Negative 
m248/17  No  Zoo  Maned wolf  Chrysocyon brachyurus  Negative 
m261/17  Yes  NA  Black owler monkey  Alouatta caraya  Negative 
m305/17  No  Zoo  Lowland tapirs  Tapirus terrestris  Positive Genbank MF975707 
m345/17  No  Zoo  Cougar  Puma concolor  Negative 
m379/17  Yes  NA  Black-tufted marmoset  Callithrix penicillata  Negative 
m514/17  No  Zoo  White-cheeked spider monkey  Ateles marginatus  Negative 
m520/17  No  Zoo  White-cheeked spider monkey  Ateles marginatus  Negative 
m530/17  Yes  NA  Capuchin monkey  Sapajus apella  Positive Genbank MF818035 
m539/17  Yes  NA  Monkey  NA  Negative 
m542/17  Yes  Santo Antônio do Leverger  Owl monkey  Aotus sp.  Negative 
m543/17  Yes  Santo Antônio do Leverger  Owl monkey  Aotus sp.  Negative 
m705/17  Yes  Cuiabá  Monkey  NA  Negative 
m709/17  Yes  Poconé  Giant anteater  Myrmecophaga tridactyla  Negative 
m743/17  No  Zoo  Coati  Nasua nasua  Negative 
m748/17  Yes  Poconé  Crab-eating fox  Cerdocyon thous  Negative 
m765/17  No  Zoo  Ocelot  Leopardus pardalis  Negative 
m787/17  No  Zoo  Margay  Leopardus weidii  Positive Genbank MF975706 
m809/17  Yes  Rondonópolis  Lowland tapirs  Tapirus terrestris  Positive Genbank MF975705 
m874/17  No  Zoo  Coati  Nasua nasua  Negative 
m878/17  Yes  Campo Verde  Howler monkey  Alouatta sp.  Negative 
m879/17  No  Zoo  Crab-eating fox  Cerdocyon thous  Negative 
m742/17  No  Zoo  Coati  Nasua nasua  Negative 
m721/17  No  Zoo  Coati  Nasua nasua  Negative 
m871/17  Yes  Cuiabá  Owl monkey  Aoutus azare  Negative 
m897/17  No  Zoo  Crab-eating fox  Cerdocyon thous  Negative 
m881/17  No  Zoo  Crab-eating fox  Cerdocyon thous  Negative 
m1055/17  Yes  NA  Capuchin monkey  Sapajus apella  Negative 
m1070/17  Yes  NA  Capybara  Hydrochoerus hydrochaeris  Negative 
m1126/17  Yes  Tangará da Serra  Cougar  Puma concolor  Negative 
m1153/17  No  Zoo  Crab-eating fox  Cerdocyon thous  Negative 
m1247/17  Yes  NA  Capuchin monkey  Sapajus apella  Negative 
m1248/17  Yes  NA  Capuchin monkey  Sapajus apella  Negative 
m1249/17  Yes  NA  Capuchin monkey  Sapajus apella  Negative 
m1267/17  Yes  Poconé  Capybara  Hydrochoerus hydrochaeris  Negative 
m1268/17  Yes  Poconé  Capybara  Hydrochoerus hydrochaeris  Negative 
m1269/17  Yes  Poconé  Capybara  Hydrochoerus hydrochaeris  Negative 
m1270/17  Yes  Poconé  Capybara  Hydrochoerus hydrochaeris  Negative 
m1271/17  Yes  Poconé  Capybara  Hydrochoerus hydrochaeris  Negative 
m1272/17  Yes  Poconé  Capybara  Hydrochoerus hydrochaeris  Negative 
m1290/17  Yes  Cuiabá  Owl monkey  Aoutus nigriceps  Negative 
m1309/17  Yes  Cáceres  Cougar  Puma concolor  Negative 
m1313/17  Yes  Cuiabá  Capuchin monkey  Sapajus apella  Negative 
m1327/17  Yes  NA  Black owler monkey  Alouatta caraya  Negative 
m1338/17  Yes  Cuiabá  Capuchin monkey  Sapajus apella  Negative 
m1339/17  Yes  Cuiabá  Sagui  Callithrix sp.  Negative 
a

Federal University of Mato Grosso-Cuiaba.

b

NA, not available.

Knowledge of the environment surrounding the infected humans or animals, and route of infection and mode of transmission are necessary to understand endemics in certain regions.4 Truman et al.5 described that isolates from human and armadillos are identical genetically. Thus, we suggest that the possible contact of animals of this study, which may be possible carriers of the bacillus, with other animals or with humans can disseminate the disease, the bacillus was detected in nasal swabs. Thus, we observe that the detection in wild animals may be associated with high prevalence and endemicity in the state of MT, which makes them important sources of infection. In addition, these data contribute to a better understanding of the epidemiology of leprosy.

Disclaimers

The opinions expressed by authors contributing to this journal do not necessarily reflect the opinions of the Centers for Disease Control and Prevention or the institutions with which the authors are affiliated.

Conflicts of interest

The authors declare no conflicts of interest.

Acknowledgments

The authors are grateful to CAPES for financial support through a scholarship.

References
[1]
Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância Epidemiológica. Sistema de Informação de Agravos de Notificação; 2016.
[2]
C. Avanzi, J. Del-Pozo, A. Benjak
Red squirrels in the British Isles are infected with leprosy bacilli
Science, 354 (2016), pp. 744-747 http://dx.doi.org/10.1126/science.aah3783
[3]
S.A. Woods, S.T. Cole
A family of dispersed repeats in Mycobacterium leprae
Mol Microbiol, 4 (1990), pp. 1745-1751
[4]
R.P. Turankar, M. Lavania, M. Singh, U. Sengupta, K.S.R.S. Sai, R.S. Jadhav
Presence of viable Mycobacterium leprae in environmental specimens around houses of leprosy patients
Indian J Med Microbiol, 34 (2016), pp. 315-321 http://dx.doi.org/10.4103/0255-0857.188322
[5]
R.W. Truman, S. Pushpendra, R. Sharma
Probable zoonotic leprosy in the southern United States
N Engl J Med, 364 (2011), pp. 1626-1633 http://dx.doi.org/10.1056/NEJMoa1010536
Copyright © 2018. Sociedade Brasileira de Infectologia
The Brazilian Journal of Infectious Diseases

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