, Volume 14, Issue 4, pp 743–749 | Cite as

Armillifer-Infected Snakes Sold at Congolese Bushmeat Markets Represent an Emerging Zoonotic Threat

  • Richard Hardi
  • Gergely Babocsay
  • Dennis Tappe
  • Mihály Sulyok
  • Imre Bodó
  • Lajos RózsaEmail author
Original Contribution


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.


Armillifer 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.


  1. Aka NA, Adoubryn K, Rondelaud D, Dreyfuss G (2008) Human paragonimiasis in Africa. Annals of African Medicine 7:153–162. doi: 10.4103/1596-3519.55660 CrossRefPubMedGoogle Scholar
  2. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575–583. doi: 10.2307/3284227 CrossRefPubMedGoogle Scholar
  3. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: Important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19:531–545. doi: 10.1128/CMR.00017-06 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Changula K, Kajihara M, Mweene AS, Takada A (2014) Ebola and Marburg virus diseases in Africa: Increased risk of outbreaks in previously unaffected areas? Microbiology and Immunology 58:483–491. doi: 10.1111/1348-0421.12181 CrossRefPubMedGoogle Scholar
  5. 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
  6. 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
  7. Dakubo J, Naaeder S, Kumodji R (2008) Totemism and the transmission of human pentastomiasis. Ghana Medical Journal 42:165–168.PubMedPubMedCentralGoogle Scholar
  8. de Merode E, Homewood K, Cowlishaw G 2004. The value of bushmeat and other wild foods to rural households living in extreme poverty in Democratic Republic of Congo. Biological Conservation 118: 573–581. doi: 10.1016/j.biocon.2003.10.005 CrossRefGoogle Scholar
  9. Edwards DP, Sloan S, Weng L, Dirks P, Sayer J, Laurance WF (2014) Mining and the African environment. Conservation Letters 7:302–311. doi: 10.1111/conl.12076 CrossRefGoogle Scholar
  10. Fa JE, Currie D, Meeuwig J (2003) Bushmeat and food security in the Congo Basin: linkages between wildlife and people’s future. Environmental Conservation 30:71–78. doi: 10.1017/S0376892903000067 CrossRefGoogle Scholar
  11. 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
  12. Karesh WB, Noble E (2009) The bushmeat trade: increased opportunities for transmission of zoonotic disease. Mount Sinai Journal of Medicine 76:429–434. doi: 10.1002/msj.20139 CrossRefPubMedGoogle Scholar
  13. Laurance WF, Croes BM, Tchignoumba L, Lahm S, Alonso A, Lee ME, Campbell P, Ondzeano C (2006) Impacts of roads and hunting on Central African rainforest mammals. Conservation Biology 20:125 –1261. doi: 10.1111/j.1523-1739.2006.00420.x CrossRefGoogle Scholar
  14. Lavrov DV, Brown WM, Boore JL (2004) Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proceedings of the Royal Society B: Biological Sciences 271:537–544. doi: 10.1098/rspb.2003.2631 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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
  16. Nasi R, Taber A, Van Vliet I 2011. Empty forests, empty stomachs? Bushmeat and livelihoods in the Congo and Amazon Basins. International Forestry Review 13:355–368. doi: 10.1505/146554811798293872 CrossRefGoogle Scholar
  17. 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
  18. Pantchev N, Tappe D (2011) Pentastomiasis and other parasitic zoonoses from reptiles and amphibians. Berliner und Münchener tierärztliche Wochenschrift 124:528–535.PubMedGoogle Scholar
  19. Reiczigel J, Rózsa L, Reiczigel A, Fábián I (2013) Quantitative Parasitology (QPweb). Available: [accessed January 11, 2017]
  20. Reiczigel J (2003) Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22:611–621. doi: 10.1002/sim.1320 CrossRefPubMedGoogle Scholar
  21. Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86:228–232. doi: 10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2 CrossRefPubMedGoogle Scholar
  22. Ruggiero MA, Gordon DP, Orrell TM, Bailly N, Bourgoin T, Brusca RC, Cavalier-Smith T, Guiry MD, Kirk PM (2015) A higher level classification of all living organisms. PLoS ONE 10(4):e0119248. doi: 10.1371/journal.pone.0119248 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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
  24. Sulyok M, Rózsa L, Bodó I, Tappe D, Hardi R (2014) Ocular pentastomiasis in the Democratic Republic of the Congo. PLoS Neglected Tropical Diseases 8:e3041. doi: 10.1371/journal.pntd.0003041 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Tappe D, Büttner DW (2009) Diagnosis of human visceral pentastomiasis. PLoS Neglected Tropical Diseases 3(2):e320. doi: 10.1371/journal.pntd.0000320 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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
  27. Tappe D, Sulyok M, Rózsa L, Muntau B, Haeupler A, Bodó I, Hardi R (2015) Molecular diagnosis of abdominal Armillifer grandis pentastomiasis in the Democratic Republic of Congo. Journal of Clinical Microbiology 53:2362–2364. doi: 10.1128/JCM.00336-15 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Wilkie DS, Sidle JG, Boundzanga GC (1992) Mechanized logging, market hunting, and a bank loan in Congo. Conservation Biology 6:570–580. doi: 10.1046/j.1523-1739.1992.06040570.x CrossRefGoogle Scholar

Copyright information

© EcoHealth Alliance 2017

Authors and Affiliations

  1. 1.St. Raphael Ophthalmological CenterMbuji MayiDemocratic Republic of the Congo
  2. 2.Mátra Museum of the Hungarian Natural History MuseumGyöngyösHungary
  3. 3.Bernhard Nocht InstituteHamburgGermany
  4. 4.Eberhard Karls UniversityTübingenGermany
  5. 5.Emory University School of MedicineAtlantaUSA
  6. 6.MTA-ELTE-MTM Ecology Research GroupBudapestHungary
  7. 7.Evolutionary Systems Research GroupMTA Centre for Ecological ResearchTihanyHungary

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