Armillifer-Infected Snakes Sold at Congolese Bushmeat Markets Represent an Emerging Zoonotic Threat
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African pythons (Pythonidae) and large vipers (Bitis spp.) act as definitive hosts for Armillifer armillatus and Armillifer grandis parasites (Crustacea: Pentastomida) in the Congo Basin. Since the proportion of snakes in bushmeat gradually increases, human pentastomiasis is an emerging zoonotic disease. To substantiate the significance of this threat, we surveyed snakes offered for human consumption at bushmeat markets in the Kole district, Democratic Republic of the Congo, for the presence of adult pentastomids. In Bitis vipers (n = 40), Armillifer spp. infestations exhibited an 87.5% prevalence and 6.0 median intensity. Parasite abundance covaried positively with viper length, but not with body mass. In pythons (n = 13), Armillifer spp. exhibited a 92.3% prevalence and 3.5 median intensity. The positive correlations between parasite abundance and python length or mass were statistically nonsignificant. Ninety-one percent of A. grandis were discovered in vipers and 97% of infected vipers hosted A. grandis, whereas 81% of A. armillatus specimens were found in pythons and 63% of infected pythons hosted A. armillatus. Thus, challenging the widespread notion of strict host specificity, we found ‘reversed’ infections and even a case of coinfection. In this study, we also gathered information about the snake consumption habits of different tribal cultures in the area. Infective parasite ova likely transmit to humans directly by consumption of uncooked meat, or indirectly through contaminated hands, kitchen tools or washing water.
KeywordsArmillifer spp. Zoonosis Congo Basin Bushmeat Python spp. Bitis spp.
We thank András Hajdú D. for the photograph. The work of Lajos Rozsa was supported by grants from the National Scientific Research Fund of Hungary (OTKA/NKFI Grant No. 108571) and GINOP-2.3.2-15-2016-00057.
Compliance with Ethical Standards
All procedures were in accordance with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. More specifically, no reptile was killed for the purpose of the present study. All information about tribal knowledge and beliefs of local people were obtained though informal conversations with illiterate local people who gave their verbal consent to recite what they told us. Therefore, no ethics committee review was required.
Conflict of interest
All the authors declare that they have no conflict of interest.
- Chifundera Kusamba Z, Nagy ZT, Kielgast J, Collet M, Mebert K, Gvozdik V (2014) Reptiles and amphibians as bushmeat in the Democratic Republic of the Congo. In: Abstracts Resumés. Anonymous (editor) 1st International Conference on Biodiversity in the Congo Basin, Centre de Surveillance de la Biodiversité, Kisangani, Democratic Republic of Congo, pp 186–187Google Scholar
- Christoffersen ML, De Assis JE (2013) A systematic monograph of the Recent Pentastomida, with a compilation of their host. Zoologische Mededelingen 87:1–206.Google Scholar
- Jackson K, Zassi-Boulou A-G, Mavoungou L-B, Pangou S (2007) Amphibians and reptiles of the Lac Télé Community Reserve, Likouala Region, Republic of Congo (Brazzaville). Herpetological Conservation and Biology 2:75–86.Google Scholar
- Magnino S, Colin P, Dei-Cas E, Madsen M, McLauchlin J, Nöckler K, Maradona MP, Tsigarida E, Vanopdenbosch E, Van Peteghem C (2009) Biological risks associated with consumption of reptile products. International Journal of Food Microbiology 134:163–75. doi: 10.1016/j.ijfoodmicro.2009.07.001 CrossRefPubMedGoogle Scholar
- Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P. (2009) Strongyloidiasis – the most neglected of the neglected tropical diseases? Transactions of the Royal Society of Tropical Medicine and Hygiene 103:967–972. doi: 10.1016/j.trstmh.2009.02.013 CrossRefPubMedGoogle Scholar
- Reiczigel J, Rózsa L, Reiczigel A, Fábián I (2013) Quantitative Parasitology (QPweb). Available: http://www2.univet.hu/qpweb/qp10/index.php [accessed January 11, 2017]
- Schmidt KP (1923) Contributions to the herpetology of the Belgian Congo based on the collection of the American Museum Congo Expedition, 1909–1915. Part II. Snakes, with field notes by Herbert Lang and James P. Chapin. Bulletin of the American Museum of Natural History 49:1–146.Google Scholar
- Tappe D, Sulyok M, Riu T, Rózsa L, Bodó I, Schoen C, Muntau B, Babocsay G, Hardi R (2016) Coinfections with Armillifer grandis, A. armillatus and Raillietiella sp. in visceral pentastomiasis, Democratic Republic of the Congo. Emerging Infectious Diseases 22:1333–1339. doi: 10.3201/eid2208.151895 CrossRefPubMedPubMedCentralGoogle Scholar