First Record of Spirometra erinaceieuropaei spargana Infection in Amphibians of South Asia: A Causative Agent of Surficial Abnormalities
-
Praneeth Silva
,
Tharanga Dasanayake
,
Dulan Jayasekara
,
Chathuranga Dharmarathne
,
Dharshani Mahaulpatha
Abstract
Background: Sparganosis is a zoonotic disease caused by Plerocercoid larvae (spargana) of the genus Spirometra. We aimed to provide molecular evidence for the infection of amphibians with Spirometra sp. in the inside and outside of Horton Plains National Park (HPNP), Sri Lanka.
Methods: The prevalence of sparganum infection in wild frogs (Truga eques and Minverya agricola) was investigated in the inside and outside of HPNP from June 2019 to April 2021.A total of 1,434 Amphibians samples were surveyed to examine the spargana infection from the study site. To identify the species identity of the collected spargana, a portion of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene and nuclear 18S rRNA gene were amplified, sequenced, and analyzed.
Results: A total of 539 infected amphibians (T. eques and M. agricola) samples were examined to survey from the study area. Spargana were detected in all dissected specimens belonging to the species Spirometra erinaceieuropaei that were genetically confirmed using the evolutionary conserved nuclear 18S rRNA gene and then compared to the GenBank deposit, indicating that S. erinaceieuropaei is the primary causal agent of sparganosis both inside and outside the HPNP.
Conclusion: Our finding is the first genetically confirmed record of S. erinaceieuropaei in amphibians in South Asia. However, further studies are needed to investigate the prevalence of sparagna infection in amphibians all over the island.
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23. Okamoto M, Iseto C, Shibahara T, et al. Intraspecific variation of Spirometra erina-ceieuropaei and phylogenetic relationship be-tween Spirometra and Diphyllobothrium in-ferred from mitochondrial CO1 gene se-quences. Parasitol Int. 2007;56(3):235-8.
24. Lunde KB, Johnson PT. A practical guide for the study of malformed amphibians and their causes. J. Herpetol. 2012;46(4):429-441.
25. Jongthawin J, Intapan PM, Sanpool O, et al. Molecular evidence of Spirometra erina-ceieuropaei infection in snakes Ptyas korros from Lao PDR and Thailand and Frogs Hoplobatrachus rugulosus from Myanmar. Southeast Asian J Trop Med Public Health. 2014;45(6):1271-1278.
26. Miller DL, Bursey CR, Gray MJ, et al. Met-acercariae of Clinostomum attenuatum in Ambystoma tigrinum mavortium, Bufo cognatus and Spea multiplicata from west Texas. J Helminthol. 2004;78(4):373-376.
27. Kondzior E, Tokarska M, Kowalczyk R, et al. The first case of genetically confirmed sparganosis (Spirometra erinaceieuropaei) in European reptiles. Parasitol. Res. 2018;117(11):3659–3662.
28. Kołodziej-Sobocińska M, Tokarska M, Kowalczyk R. The first report of sparga-nosis (Spirometra sp.) in Eurasian badger (Meles meles). Parasitol Int. 2014; 63(2):397–399.
29. Nithiuthai S, Anantaphruti MT, Waikagul J, et al. Waterborne zoonotic helminthiases. Vet Parasitol. 2004;126(1):167–193.
30. Liu W, Liu GH, Li F, et al. Sequence varia-bility in three mitochondrial DNA regions of Spirometra erinaceieuropaei spargana of human and animal health significance. J Helminthol. 2012;86(3):271-5.
31. Steenkiste Van, Locke N, Castelin S A, et al. New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Mol Ecol Resour. 2015;15(4) :945-952.
32. Liu Q, Li MW, Wang ZD, et al. Human sparganosis, a neglected food borne zo-onosis. Lancet Infect Dis. 2015;15(10):1226–1235.
33. Wang F, Zhou L, Gong S, et al.Severe in-fection of wild-caught snakes with Spi-rometra erinaceieuropaei from food mar-kets in Guangzhou, China involves a risk for zoonotic sparganosis. J Parasitol. 2011;97(1):170–171.
2. Reeves MK, Dolph CL, Zimmer H, et al. Road proximity increases risk of skeletal abnormalities in wood frogs from Nation-al Wildlife Refuges in Alaska. Environ Health Perspect. 2008;116(8):1009-1014.
3. Sahoo N, Sahoo S, Mohanty B, et al. Mo-lecular identification of Spirometra erina-ceieuropaei infection in a dog with its suc-cessful treatment. J Entomol Zool. 2018;6(4):1487-1489.
4. Gray ML, Rogers F, Little S, et al. Sparga-nosis in feral hogs (Sus scrofa) from Florida. J Am Vet Med Assoc. 1999;215: 204-8.
5. Zhu X, Beveridge I, Berger L, et al. Single strand conformation polymorphism-based analysis reveals genetic variation within Spirometra erinacei (Cestoda: Pseudo-phyllidea) from Australia. Mol Cell Probes. 2002;16(2):159–16.
6. Kołodziej-Sobocińska M, Miniuk M, Ruczyńska I, et al. Sparganosis in wild boar (Sus scrofa) – implications for veterinarians, hunters, and consumers. Vet Parasi-tol.2016;227:115–117.
7. Anantaphruti MT, Nawa Y, Vanvanitchai Y. Human sparganosis in Thailand: an overview. Acta Trop. 2011;118(3):171-176.
8. Mueller JF. The biology of Spirometra. J Parasitol. 1974;60(1): 3-14.
9. Wongkulab P, Sukontason K, Chaiwarith R. Sparganosis: a brief review. J Infect Dis Antimicrob Agents. 2011;28:77–80.
10. Hong Q, Feng JP, Liu HJ, et al. Prevalence of Spirometra mansoni in dogs, cats, and frogs and its medical relevance in Guang-zhou, China. Int J Infect Dis. 2016; 53:41–45.
11. Silva GKVPT, Mahaulpatha WAD, de Sil-va A. Amphibian abnormalities and threats in pristine ecosystems in Sri Lanka. J Threat Taxa. 2019;11(15):15004-15014.
12. Nakao M, Sako Y, Yokoyama N, et al. Mitochondrial genetic code in cestodes. Mol Biochem Parasitol. 2000;111(2):415–424.
13. Nelli S, Felix D, Marine A. Seven new spe-cies of helminths for reptiles from Arme-nia. Acta Parasitol. 2014; 59(3):442–447.
14. Cui J, Li N, Wang ZQ, et al. Serodiagnosis of experimental sparganum infections of mice and human sparganosis by ELISA using ES antigens of Spirometra mansoni spargana. Parasitol Res. 2011;108(6):1551–1556.
15. Linder G. Multiple stressor effects in rela-tion to declining amphibian populations. J ASTM Int. 2003;1443:3-262
16. Blaustein AR, Johnson PT. The complexity of deformed amphibians. Front Ecol En-viron. 2003;1(2):87-94.
17. Ankley GT, Degitz SJ, Diamond SA, et al. Assessment of environmental stressors potentially responsible for malformations in North American anuran amphibians. Ecotoxicol Environ Saf. 2004;58(1):7-16.
18. Imasuen AA, Ozemoka HJ, Aisien MS. Anurans as intermediate and paratenic hosts of helminth infections in the rain-forest and derived savanna biotopes of southern Nigeria. Int J Zool. 2012;5(3):1-7.
19. Liu W, Zhao GH, Tan MY, et al. Survey of Spirometra erinaceieuropaei spargana infection in the frog Rana nigromaculata of the Hunan Province of China. Vet Parasitol. 2010;173:152-6.
20. Lescano AG, Zunt J. Other cestodes: sparganosis, coenurosis and Taenia crassiceps cys-ticercosis. Handb Clin Neurol. 2013;1(114):335-45.
21. Ooi HK, Chang SL, Huang CC, et al. Sur-vey of Spirometra erinaceieuropaei in frogs in Taiwan and its experimental infection in cats. J Helminthol. 2000;74(2):173-6.
22. Scholz T, Kuchta R, Brabec J. Broad tape-worms (Diphyllobothriidae), parasites of wildlife and humans: Recent progress and future challenges. Int J Parasitol Parasites Wildl. 2019;9:359-369.
23. Okamoto M, Iseto C, Shibahara T, et al. Intraspecific variation of Spirometra erina-ceieuropaei and phylogenetic relationship be-tween Spirometra and Diphyllobothrium in-ferred from mitochondrial CO1 gene se-quences. Parasitol Int. 2007;56(3):235-8.
24. Lunde KB, Johnson PT. A practical guide for the study of malformed amphibians and their causes. J. Herpetol. 2012;46(4):429-441.
25. Jongthawin J, Intapan PM, Sanpool O, et al. Molecular evidence of Spirometra erina-ceieuropaei infection in snakes Ptyas korros from Lao PDR and Thailand and Frogs Hoplobatrachus rugulosus from Myanmar. Southeast Asian J Trop Med Public Health. 2014;45(6):1271-1278.
26. Miller DL, Bursey CR, Gray MJ, et al. Met-acercariae of Clinostomum attenuatum in Ambystoma tigrinum mavortium, Bufo cognatus and Spea multiplicata from west Texas. J Helminthol. 2004;78(4):373-376.
27. Kondzior E, Tokarska M, Kowalczyk R, et al. The first case of genetically confirmed sparganosis (Spirometra erinaceieuropaei) in European reptiles. Parasitol. Res. 2018;117(11):3659–3662.
28. Kołodziej-Sobocińska M, Tokarska M, Kowalczyk R. The first report of sparga-nosis (Spirometra sp.) in Eurasian badger (Meles meles). Parasitol Int. 2014; 63(2):397–399.
29. Nithiuthai S, Anantaphruti MT, Waikagul J, et al. Waterborne zoonotic helminthiases. Vet Parasitol. 2004;126(1):167–193.
30. Liu W, Liu GH, Li F, et al. Sequence varia-bility in three mitochondrial DNA regions of Spirometra erinaceieuropaei spargana of human and animal health significance. J Helminthol. 2012;86(3):271-5.
31. Steenkiste Van, Locke N, Castelin S A, et al. New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Mol Ecol Resour. 2015;15(4) :945-952.
32. Liu Q, Li MW, Wang ZD, et al. Human sparganosis, a neglected food borne zo-onosis. Lancet Infect Dis. 2015;15(10):1226–1235.
33. Wang F, Zhou L, Gong S, et al.Severe in-fection of wild-caught snakes with Spi-rometra erinaceieuropaei from food mar-kets in Guangzhou, China involves a risk for zoonotic sparganosis. J Parasitol. 2011;97(1):170–171.
| Files | ||
| Issue | Vol 17 No 3 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v17i3.10631 | |
| Keywords | ||
| Horton plains national park (HPNP); Spargana Sparganosis Spirometra erinaceieuropaei | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Silva P, Dasanayake T, Jayasekara D, Dharmarathne C, Mahaulpatha D. First Record of Spirometra erinaceieuropaei spargana Infection in Amphibians of South Asia: A Causative Agent of Surficial Abnormalities. Iran J Parasitol. 2022;17(3):402-409.
