Zoonotic Parasites of Reptiles: A Crawling Threat
Language English Country Great Britain, England Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Review
PubMed
32448703
PubMed Central
PMC7203055
DOI
10.1016/j.pt.2020.04.014
PII: S1471-4922(20)30128-8
Knihovny.cz E-resources
- Keywords
- food-borne, pentastomiasis, reptile pet trade, sparganosis, vector-borne, zoonotic parasites,
- MeSH
- Pets parasitology MeSH
- Humans MeSH
- Parasitic Diseases parasitology prevention & control transmission MeSH
- Parasites MeSH
- Reptiles parasitology MeSH
- Food Parasitology MeSH
- Zoonoses parasitology prevention & control MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
Reptiles are reservoirs of a wide range of pathogens, including many protozoa, helminths, pentastomids, and arthropod parasitic species, some of which may be of public health concern. In this review we discuss the zoonotic risks associated with human-reptile interactions. Increased urbanization and introduction of exotic species of reptile may act as drivers for the transmission of zoonotic parasites through the environment. In addition, being a part of human diet, reptiles can be a source of life-threatening parasitoses, such as pentastomiasis or sparganosis. Finally, reptiles kept as pets may represent a risk to owners given the possibility of parasites transmitted by direct contact or fecal contamination. Awareness of reptile-borne zoonotic parasitoses is important to advocate control, prevention, and surveillance of these neglected diseases.
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Pincheira-Donoso D. Global taxonomic diversity of living reptiles. PLoS One. 2013;8:3. PubMed PMC
Alves R., Albuquerque U., editors. Ethnozoology: Animals in Our Lives. Academic Press; 2018.
Engler M., Parry-Jones R., editors. Opportunity or Threat: The Role of the European Union in Global Wildlife Trade. TRAFFIC Europe; 2007.
Mitchell M. Zoonotic diseases associated with reptiles and amphibians: an update. Vet. Clin. North. Am. Exot. Anim. Pract. 2011;14:439–456. PubMed
Corrente M. Risk for zoonotic Salmonella transmission from pet reptiles: a survey on knowledge, attitudes and practices of reptile-owners related to reptile husbandry. Prev. Vet. Med. 2017;146:73–78. PubMed
Bower D. A review of the role of parasites in the ecology of reptiles and amphibians. Austral. Ecol. 2019;44:433–448.
Wolfe K. Does urbanization influence the diet of a large snake? Curr. Zool. 2017;64:311–318. PubMed PMC
French S. Town and country reptiles: a review of reptilian responses to urbanization. Integr. Comp. Biol. 2018;58:948–966. PubMed
Kelehear C. Invasive parasites in multiple invasive hosts: the arrival of a new host revives a stalled prior parasite invasion. Oikos. 2013;122:1317–1324.
Reboredo-Fernández A. Detection of zoonotic and livestock-specific assemblages of Giardia duodenalis in free-living wild lizards. Rev. Bras. Parasitol. Vet. 2017;26:395–399. PubMed
Hoyer J. Mammal decline, linked to invasive Burmese python, shifts host use of vector mosquito towards reservoir hosts of a zoonotic disease. Biology. 2017;13:10. PubMed PMC
Miller A. Parasite spillover: indirect effects of invasive Burmese pythons. Ecol. Evol. 2018;8:830–840. PubMed PMC
Dakubo J. Totemism and the transmission of human pentastomiasis. Ghana Med. J. 2008;42:165. PubMed PMC
Westfall A. Host-specific phenotypic variation of a parasite co-introduced with invasive Burmese pythons. PLoS One. 2019;14:1. PubMed PMC
Italiano C. Sarcocystis nesbitti causes acute, relapsing febrile myositis with a high attack rate: description of a large outbreak of muscular sarcocystosis in Pangkor Island, Malaysia, 2012. PLoS Negl. Trop. Dis. 2014;8:5. PubMed PMC
Lau Y. Sarcocystis nesbitti infection in human skeletal muscle: possible transmission from snakes. Am. J. Trop. Med. Hyg. 2014;90:361–364. PubMed PMC
Fayer R. Human infections with Sarcocystis species. Clin. Microbiol. Rev. 2015;28:295–311. PubMed PMC
Yared S. A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host–vector system. Heliyon. 2019;5:7. PubMed PMC
Bosco-Lauth A. Reptiles and amphibians as potential reservoir hosts of Chikungunya virus. Am. J. Trop. Med. Hyg. 2018;98:841–844. PubMed PMC
Tsujimoto Y. Necrotizing fasciitis and sepsis caused by Aeromonas hydrophila. Infez. Med. 2019;4:21. PubMed
Kwon J. A case of mortality caused by Aeromonas hydrophila in wild-caught red-eyed crocodile skinks (Tribolonotus gracilis) Vet. Sci. 2020;7:4. PubMed PMC
Krishnavajhala A. Vector competence of geographical populations of Ornithodoros turicata for the tick-borne relapsing fever spirochete Borrelia turicatae. Appl. Environ. Microbiol. 2018;84:5–18. PubMed PMC
Campbell S. Evaluating the risk of tick-borne relapsing fever among occupational cavers-Austin, TX, 2017. Zoonoses Public Health. 2019;66:579–586. PubMed PMC
Brianti E. Risk for the introduction of exotic ticks and pathogens into Italy through the illegal importation of tortoises, Testudo graeca. Med. Vet. Entomol. 2010;24:336–339. PubMed
Paștiu A. Zoonotic pathogens associated with Hyalomma aegyptium in endangered tortoises: evidence for host-switching behaviour in ticks? Parasit. Vectors. 2012;5:301. PubMed PMC
Široký P. Hidden threat of tortoise ticks: high prevalence of Crimean-Congo haemorrhagic fever virus in ticks Hyalomma aegyptium in the Middle East. Parasit. Vectors. 2014;7:101. PubMed PMC
Barradas P. Pathogenic Rickettsia in ticks of spur – thighed tortoise (Testudo graeca) sold in a Qatar live animal market. Transbound. Emerg. Dis. 2019;67:461–465. PubMed
Široký P. Tortoise tick Hyalomma aegyptium as long term carrier of Q fever agent Coxiella burnetii – evidence from experimental infection. Parasitol. Res. 2010;107:1515–1520. PubMed
Novakova M. Rickettsial infections in ticks from reptiles, birds and humans in Honduras. Ticks Tick Borne Dis. 2015;6:737–742. PubMed
Mediannikov O. Rickettsia africae, western Africa. Emerg. Infect. Dis. 2010;16:571. PubMed PMC
Burridge M., Simmons L. Exotic ticks introduced into the United States on imported reptiles from 1962 to 2001 and their potential roles in international dissemination of diseases. Vet. Parasitol. 2003;113:289–320. PubMed
Unsworth N. Flinders Island spotted fever rickettsioses caused by 'marmionii' strain of Rickettsia honei, Eastern Australia. Emerg. Infect. Dis. 2007;13:566. PubMed PMC
Whiley H. Rickettsia detected in the reptile tick Bothriocroton hydrosauri from the lizard Tiliqua rugosa in South Australia. Pathogens. 2016;5:41. PubMed PMC
Reeves W. A spotted fever group Rickettsia from an exotic tick species, Amblyomma exornatum (Acari: Ixodidae), in a reptile breeding facility in the United States. J. Med. Entomol. 2006;43:1099–1101. PubMed
Mendoza-Roldan J. Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy. Parasit. Vectors. 2019;12:35. PubMed PMC
Bravo-Barriga D. First molecular detection of Leishmania tarentolae-like DNA in Sergentomyia minuta in Spain. Parasitol. Res. 2016;115:1339–1344. PubMed
Campino L. The first detection of Leishmania major in naturally infected Sergentomyia minuta in Portugal. Mem. Inst. Oswaldo Cruz. 2013;108:516–518. PubMed PMC
Pereira S. First molecular detection of Leishmania infantum in Sergentomyia minuta (Diptera, Psychodidae) in Alentejo, southern Portugal. Acta Trop. 2017;174:45–48. PubMed
Latrofa M. Detection of Leishmania infantum DNA in phlebotomine sand flies from an area where canine leishmaniosis is endemic in southern Italy. Vet. Parasitol. 2018;253:39–42. PubMed
Zhang J. Molecular detection, identification and phylogenetic inference of Leishmania spp. in some desert lizards from Northwest China by using internal transcribed spacer 1 (ITS1) sequences. Acta Trop. 2016;162:83–94. PubMed
Zhang J. Pathogenic Leishmania spp. detected in lizards from Northwest China using molecular methods. BMC Vet. Res. 2019;15:446. PubMed PMC
Valencia-Aguilar A. Ecosystem services provided by amphibians and reptiles in Neotropical ecosystems. J. Biodivers. Sci. Ecosyst. Serv. Manag. 2013;9:257–272.
Greiner E. Coccidiosis in reptiles. Semin. Avian Exot. Pet Med. 2003;12:49–56.
Patro S., Padhi S. Saltwater crocodile and human conflict around Bhitarkanika National Park, India: a raising concern for determining conservation limits. Ocean Coast. Manag. 2019;182:104923.
Hossain M. Food consumption of saltwater crocodile (Crocodylus porosus) in a reptile farm of Bangladesh. Bangladesh J. Zool. 2013;41:173–179.
Bulte E. Resource intensity, institutions, and development. World Dev. 2005;33:1029–1044.
Magnino S. Biological risks associated with consumption of reptile products. Int. J. Food Microbiol. 2009;134:163–175. PubMed
Kwon J., Kim J. Sparganosis presenting as a conus medullaris lesion: case report and literature review of the spinal sparganosis. Arch. Neurol. 2004;61:1126–1128. PubMed
Presti A. Cerebral sparganosis: case report and review of the European cases. Acta Neurochir. 2015;157:1339–1343. PubMed
Liu L. Serodiagnosis of sparganosis by ELISA using recombinant cysteine protease of Spirometra erinaceieuropaei spargana. Parasitol. Res. 2015;114:753–757. PubMed
Anantaphruti M. Human sparganosis in Thailand: an overview. Acta Trop. 2011;118:171–176. PubMed
Liu Q. Human sparganosis, a neglected food borne zoonosis. Lancet Infect. Dis. 2015;15:1226–1235. PubMed
Barratt J. Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology. 2016;143:1087–1118. PubMed
Prociv P. Neuro-angiostrongyliasis: unresolved issues. Int. J. Parasitol. 2000;30:1295–1303. PubMed
Parameswaran K. Case series of eosinophilic meningoencephalitis from South India. Ann. Indian Acad. Neurol. 2006;9:217.
Johny J. Eosinophilic meningitis caused by consumption of meat of monitor lizard (Varanus bengalensis) Neurol. India. 2018;66:1166. PubMed
Pozio E. Trichinella papuae and Trichinella zimbabwensis induce infection in experimentally infected varans, caimans, pythons and turtles. Parasitology. 2004;128:333. PubMed
Pozio E. Trichinella papuae in saltwater crocodiles (Crocodylus porosus) of Papua New Guinea. Emerg. Infect. Dis. 2004;10:1507–1509. PubMed PMC
Paré J. An overview of pentastomiasis in reptiles and other vertebrates. J. Exot. Pet Med. 2008;17:285–294.
Chen S.-H. Multi-host model-based identification of Armillifer agkistrodontis (Pentastomida), a new zoonotic parasite from China. PLoS Negl. Trop. Dis. 2010;4:647. PubMed PMC
du Plessis V. Pentastomiasis (Armillifer armillatus infestation) S. Afr. Med. J. 2007;97:928–930. PubMed
Tappe D., Büttner D. Diagnosis of human visceral pentastomiasis. PLoS Negl. Trop. Dis. 2009;3 PubMed PMC
Tappe D. Imported Armillifer pentastomiasis: Report of a symptomatic infection in The Netherlands and mini-review. Travel Med. Infect. Dis. 2014;12:129–133. PubMed
Tappe D. Transmission of Armillifer armillatus ova at snake farm, The Gambia, West Africa. Emerg. Infect. Dis. 2011;17:251. PubMed PMC
Yapo H. Human pentastomiasis discovered post-mortem. Forensic Sci. Int. 2003;137:52–54. PubMed
Burns-Cox C. Porocephaliasis in Western Malaysia. Trans. R. Soc. Trop. Med. Hyg. 1969;63:409–411. PubMed
Pantchev N., Tappe D. Pentastomiasis and other parasitic zoonoses from reptiles and amphibians. Berl. Munch. Tierarztl. 2011;124:528–535. PubMed
Rataj A. Parasites in pet reptiles. Acta Vet. Scand. 2011;53:33. PubMed PMC
Schuppli C. Welfare of non-traditional pets. Rev. Sci. Tech. 2014;33:221–231. PubMed
Pasmans F. Future of keeping pet reptiles and amphibians: towards integrating animal welfare, human health and environmental sustainability. Vet. Rec. 2017;181:7. PubMed
Cervone M. Internal and external parasitic infections of pet reptiles in Italy. J. Herpetol. Med. Surg. 2016;26:122–130.
Chomel B. Wildlife, exotic pets, and emerging zoonoses. Emerg. Infect. Dis. 2007;13:6. PubMed PMC
Mader D., Divers S., editors. Current Therapy in Reptile Medicine and Surgery. Elsevier Health Sciences; 2013.
Nowak M. The international trade in reptiles (Reptilia) – the cause of the transfer of exotic ticks (Acari: Ixodida) to Poland. Vet. Parasitol. 2010;169:373–381. PubMed
Traversa D. Cryptosporidium from tortoises: genetic characterisation, phylogeny and zoonotic implications. Mol. Cell. Probe. 2008;22:122–128. PubMed
Rinaldi L. Prevalence and molecular identification of Cryptosporidium isolates from pet lizards and snakes in Italy. Parasite. 2012;19:437. PubMed PMC
Pedraza-Díaz S. Molecular characterisation of Cryptosporidium isolates from pet reptiles. Vet. Parasitol. 2009;160:204–210. PubMed
Díaz P. Cryptosporidium in pet snakes from Italy: molecular characterization and zoonotic implications. Vet. Parasitol. 2013;197:68–73. PubMed
Galecki R. Tongue worm (Pentastomida) infection in ball pythons (Python regius) – a case report. Ann. Parasitol. 2016;62:363–365. PubMed
Lyons J., Natusch D. AC28 Inf. Vol. 9. IUCN-SSC Boa and Python Specialist Group; 2015. Methodologies for differentiating between wild and captive-bred CITES-listed snakes; p. 35.
Wolf D. Diagnosis of gastrointestinal parasites in reptiles: comparison of two coprological methods. Acta Vet. Scand. 2014;56:44. PubMed PMC
Decaro N. COVID-19 from veterinary medicine and One Health perspectives: What animal coronaviruses have taught us. Res. Vet. Sci. 2020;131:21–23. PubMed PMC
Tappe D., Warrell D. Pentastomiasis. In: Ryan E.T., editor. Hunter's Tropical Medicine and Emerging Infectious Diseases. Elsevier; 2019. pp. 1030–1032.
Boomker J. Eustrongylides sp. (Nematoda: Dioctophymatoidea) from the stomach of a Nile crocodile, Crocodylus niloticus Laurenti, 1768, in Botswana: research communication. Onderstepoort J. Vet. Res. 2006;73:315–317. PubMed
Nawa Y. Ocular gnathostomiasis – update of earlier survey. Am. J. Trop. Med. Hyg. 2017;97:1232–1234. PubMed PMC
Eamsobhana P. Review paper eosinophilic meningitis caused by Angiostrongylus cantonensis – a neglected disease with escalating importance. Trop. Biomed. 2014;31:569–578. PubMed
Pauwels O., Pantchev N. Risks for human health related to invasive alien reptiles and amphibians. In: Mazza G., Tricarico E., editors. Invasive Species and Human Health. CABI International; 2018. pp. 108–119.
Sánchez-Montes S. Rickettsia species in ticks that parasitize amphibians and reptiles: novel report from Mexico and review of the worldwide record. Ticks Tick Borne Dis. 2019;10:987–994. PubMed
Amanatfard E. Human dermatitis caused by Ophionyssus natricis, a snake mite. Iran. J. Parasitol. 2014;9:594. PubMed PMC
Mendoza-Roldan J. Mites and ticks of reptiles and amphibians in Brazil. Acta Trop. 2020 doi: 10.1016/j.actatropica.2020.105515. Published online May 11, 2020. PubMed DOI
Shaw G. End of Cretaceous extinction: the end of the dinosaurs. In: Shaw G., editor. Great Moments in the History of Life. Springer; 2018. pp. 65–68.
Mohabey D., Samant B. Cretaceous–paleogene transition of reptilian tetrapods across deccan volcanism in India. Open J. Geol. 2019;9:639.
Uetz P. A global catalogue of primary reptile type specimens. Zootaxa. 2019;4695:438–450. PubMed
European Food Safety Authority (EFSA) Public health risks involved in the human consumption of reptile meat – Scientific Opinion of the Panel on Biological Hazards. EFSA J. 2007;5:578.
da Nóbrega A. Reptiles used in traditional folk medicine: conservation implications. Biodivers. Conserv. 2008;17:2037–2049.
Robinson J. Dynamics of the global trade in live reptiles: Shifting trends in production and consequences for sustainability. Biol. Conserv. 2015;184:42–50.
Tavasoli E. Hyalomma aegyptium on spur-thighed tortoise (Testudo graeca) in Urmia Region West Azerbaijan, Iran. Iran. J. Parasitol. 2007;2:40–47.
Vatansever Z. Ticks biting humans in the urban area of Istanbul. Parasitol. Res. 2008;102:551–553. PubMed
Molecular evidence of Monocercomonas and Acanthamoeba in the feces of captive reptiles