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An epidemiological study of A. cantonensis in Jamaica subsequent to an outbreak of human cases of eosinophilic meningitis in 2000

Published online by Cambridge University Press:  13 April 2016

C. A. WAUGH ,
J. F. LINDO ,
J. LORENZO-MORALES  and
R. D. ROBINSON
C. A. WAUGH
Affiliation:
Department of Life Sciences, The University of the West Indies, Mona, Kingston 7, Jamaica
J. F. LINDO
Affiliation:
Department of Microbiology, The University of the West Indies, Mona, Kingston 7, Jamaica
J. LORENZO-MORALES
Affiliation:
Institute of Tropical Diseases and Public Health of the Canary Islands, The University of La Laguna, Tenerife, Canary Islands
R. D. ROBINSON*
Affiliation:
Department of Life Sciences, The University of the West Indies, Mona, Kingston 7, Jamaica
*
*Corresponding author: Department of Life Sciences, The University of the West Indies, Mona, Kingston 7, Jamaica. E-mail: [email protected]
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Summary

The infection status of angiostrongylosis in Jamaica was assessed in wild rats and molluscs in the 5 years following the major outbreak of eosinophilic meningitis (EM) in 2000. Parasitological analyses of 297 Rattus rattus and 140 Rattus norvegicus, and 777 terrestrial molluscs from all 14 Parishes on the island revealed Angiostrongylus cantonensis in 32·0% of the rats and in 12·5% of the molluscs. Multivariate analyses confirmed that A. cantonensis occurred significantly more frequently in R. rattus (Odds Ratio [OR] = 1·76), while mean infection intensity in R. rattus was also significantly higher (16·8) than R. norvegicus (11·3) (Mann–Whitney U-test: P = 0·01). Third-stage larvae of A. cantonensis were detected in 29% of 86 Pleurodonte spp.; in 20% of five Poteria spp.; in 18·7% of 369 Thelidomus asper; in 11% of 18 Sagda spp.; and in 6% of 24 veronicellid slugs. Most rodent infections occurred in Northeastern Jamaica (OR = 11·66), a region where infected molluscs were also abundant. Given the prevalence of A. cantonensis infection in rats has significantly increased since the 2000 outbreak, and that a survey of human infections revealed at least ten autochthonous cases in the last 15 years, angiostrongylosis persists as an important zoonosis in Jamaica.

Keywords

Angiostrongylus cantonensisRat lungwormRattusPleurodonteThelidomuseosinophilic meningitisemerging infectious diseaseJamaica
Type
Research Article
Information
Parasitology , Volume 143 , Issue 9 , August 2016 , pp. 1211 - 1217
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Aguiar, P. H., Morera, P. and Pascual, J. (1981). First record of Angiostrongylus cantonensis in Cuba. American Journal of Tropical Medicine and Hygiene 30, 963–965.Google Scholar
Alicata, J. E. (1969). Present status of Angiostrongylus cantonensis infection in man and animals in the tropics. Journal of Tropical Medicine and Hygiene 72, 53–63.Google ScholarPubMed
Andersen, E., Gubler, D. J., Sorenson, K., Beddard, J. and Ash, L. R. (1986). First report of Angiostrongylus cantonensis in Puerto Rico. American Journal of Tropical Medicine and Hygiene 35, 319–322.Google Scholar
Anderson, R. C., Chabaud, A. G. and Willmott, S. (2009). Keys to the Nematode Parasites of Vertebrates. p. 480 Commonwealth Agricultural Bureaux International, Wallingford, UK. ISBN-13: 978-1-84593-572-6.Google Scholar
Anderson, R. M. and Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.Google Scholar
Asato, R., Taira, K., Nakamura, M., Kudaka, J., Itokazu, K. and Kawanaka, M. (2004). Changing epidemiology of Angiostrongyliasis cantonensis in Okinawa Prefecture, Japan. Japanese Journal of Infectious Diseases 57, 184–186.Google Scholar
Ash, L. A. (1970). Diagnostic morphology of the third-stage larvae of Angiostrongylus cantonensis, Angiostrongylus vasorum, Aelurostrongylus abstrusus, and Anafilaroides rostratus (Nematoda: Metastrongyloidea). Journal of Parasitology 56, 249–253.Google Scholar
Aziz, N. A. A., Daly, E., Allen, S., Rowson, B., Greig, C., Forman, D. and Morgan, E. R. (2016). Distribution of Angiostrongylus vasorum and its gastropod intermediate hosts along the rural–urban gradient in two cities in the United Kingdom, using real time PCR. Parasites and Vectors. 9, 56. doi: 10.1186/s13071-016-1338-3.Google Scholar
Barrow, K. O., St. Rose, A. and Lindo, J. F. (1996). Eosinophilic meningitis: is Angiostrongylus cantonensis endemic in Jamaica? West Indian Medical Journal 45, 70–71.Google ScholarPubMed
Burton, M. and Burton, R. (2002). International Wildlife Encyclopedia, 3rd Edn. Marshall Cavendish, New York.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Campbell, B. G. and Little, M. D. (1988). The finding of Angiostrongylus cantonensis in rats in New Orleans. American Journal of Tropical Medicine and Hygiene 38, 568–573.Google Scholar
Chen, H. T. (1935). Un nouveau nematode pulmonaire: Pulmomema cantonensis n.g.n.spp. de rats de Canton. Annales de Parasitologie Humaine et Comparée 13, 312–317.Google Scholar
Chikweto, A., Bhaiyat, M. I., Macpherson, C. N. L., De Allie, C., Pinckney, R. D., Richards, C. and Sharma, R. N. (2009). Existence of Angiostrongylus cantonensis in rats (Rattus norvegicus) in Grenada, West Indies. Veterinary Parasitology 162, 160–162.Google Scholar
Cowie, R. H. (2013 a). Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai'i Journal of Medicine and Public Health 72(Suppl. 2), 6–9.Google Scholar
Cowie, R. H. (2013 b). Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawai'i Journal of Medicine and Public Health 72(Suppl. 2), 70–74.Google Scholar
Cowie, R. H., Hollyer, J. R., da Silva, A. J., Hollingsworth, R. G., Dixon, M. C., Eamsobhana, P., Fox, L. M., Gosnell, W. L., Howe, K., Johnson, S., Kim, J. R., Kramer, K. J., Lim, P. E., Lindo, J. F., Lun, Z.-R., Maldonado, A., Morassutti, A. L., Murphy, G. S., Park, S. Y., Qvarnstrom, Y., Robinson, R. D., Sawanyawisuth, K., Teem, J., Thiengo, S. C., Todd, C. D., Tsai, H.-C., Wallace, G. D., Waugh, C. A., Whelen, A. C., Wilkins, P. P. (2012). Workshop on research priorities for management and treatment of angiostrongyliasis. Emerging Infectious Diseases [Online]. http://dx.doi.org/10.3201/eid1812.120499.Google Scholar
De Meuron, K. (2005). Angiostrongylose en Martinique: à propos de quatre cas pédiatriques . Ph.D. thesis. Faculte de Medecine, Université de Bourgogne, France. 134 pp.Google Scholar
Evans-Gilbert, T., Lindo, J. F., Henry, S., Brown, P. and Christie, C. D. (2014). Severe eosinophilic meningitis owing to Angiostrongylus cantonensis in young Jamaican children: case report and literature review. Paediatrics and International Child Health 34, 148–152.Google Scholar
Giannelli, A., Colella, V., Abramo, F., do Nascimento-Ramos, R. A., Falsone, L., Brianti, E., Varcasia, A., Dantas-Torres, F., Knaus, M., Fox, M. T. and Otranto, D. (2015). Release of lungworm larvae from snails in the environment: potential for alternative transmission pathways. PLoS Neglected Tropical Diseases 9, e0003722. doi: 10.1371/journal.pntd.0003722.Google Scholar
Heyneman, D., and Lim, B. L. (1967). Angiostrongylus cantonensis: proof of direct transmission with its epidemiological implications. Science 158, 1057–1058.Google Scholar
Jovani, R. and Tella, J. L. (2006). Parasite prevalence and sample size: misconceptions and solutions. Trends in Parasitology 22, 214–218.CrossRefGoogle ScholarPubMed
Justine, J.-L., Winsor, L., Barrière, P., Fanai, C., Gey, D., Han, A. W. K., La Quay-Velazquez, G., Lee, B. P. Y.-H., Lefevre, J.-M., Meyer, J.-Y., Philippart, D., Robinson, D. G., Thévenot, J. and Tsatsia, F. (2015). The invasive land planarian Platydemus manokwari (Platyhelminthes, Geoplanidae): records from six new localities, including the first in the USA. PeerJ 3, e1037.CrossRefGoogle ScholarPubMed
King, C. H. (2001). PRO/AH/EDR> Eosinophilic meningitis – USA ex Jamaica. ProMED-mail post. International Society for Infectious Diseases. http://www.promedmail.org/direct.php?id=20011007.2426 +Eosinophilic+meningitis+–+USA+ex+Jamaica.+ProMED-mail+post.+International+Society+for+Infectious+Diseases.+http://www.promedmail.org/direct.php?id=20011007.2426>Google Scholar
Lindo, J. F., Waugh, C., Hall, J., Cunningham-Myrie, C., Ashley, D., Eberhard, M. L., Sullivan, J. J., Bishop, H. S., Robinson, D. G., Holtz, T. and Robinson, R. D. (2002). Enzootic Angiostrongylus cantonesis in rats and snails after an outbreak of human eosinophilic meningitis in Jamaica. Emerging Infectious Diseases 8, 324–326.Google Scholar
Lindo, J. F., Escoffery, C. T., Reid, B., Codrington, G., Cunningham-Myrie, C. and Eberhard, M. (2004). Fatal autochthonous eosinophilic meningitis in a Jamaican child caused by Angiostrongylus cantonensis . American Journal of Tropical Medicine and Hygiene 70, 425–428.Google Scholar
Lindo, J. F., Waugh, C., Todd, C., Brown, P. and Robinson, R. D. (2011). The emergence of Angiostrongylus cantonensis as a cause of eosinophilic meningitis in Jamaica: progress and pitfalls. In Angiostrongylus and Angiostrongyliasis: Advances in the Disease, Control, Diagnosis, and Molecular Genetics (ed. Eamsobhana, P.), pp. 27–31. Wattanakij Panich Press, Bangkok. ISBN 7978-974-11-1436-8.Google Scholar
Louisiana Office of Public Health (2006). Angiostrongylus cantonensis. Infectious Disease Epidemiology Section – Annual Report. http://www.dhh.state.la.us/assets/oph/Center-PHCH/Center-CH/infectious-epi/Annuals/LaIDAnnual_Angiostrongylus.pdf Google Scholar
Lv, S., Zhang, Y., Steinmann, P., Yang, G.-J., Yang, K., Zhou, X.-N. and Utzinger, J. (2011). The emergence of angiostrongyliasis in the People's Republic of China: the interplay between invasive snails, climate change and transmission dynamics. Freshwater Biology 56, 717–734.Google Scholar
Mackerras, M. J. and Sandars, D. F. (1955). The life history of the rat lungworm, Angiostrongylus cantonensis (Chen) (Nematoda: Metastrongylidae). Australian Journal of Zoology 3, 1–25.Google Scholar
Mahon, R. and Aiken, K. (1977). The establishment of the North American Bullfrog, Rana catesbeiana (Amphibia, Anura, Ranidae) in Jamaica. Journal of Herpetology 11, 197–199.Google Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. and Schad, G. A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68, 131–133.Google Scholar
Mattis, A., Mowatt, L., Lue, A., Lindo, J. F. and Vaughn, H. (2009). Ocular angiostrongyliasis - first case report from Jamaica. The West Indian Medical Journal 58, 383–385.Google Scholar
Murphy, G. S. and Johnson, S. (2013). Clinical aspects of eosinophilic meningitis and meningoencephalitis caused by Angiostrongylus cantonensis, the rat lungworm. Hawai'i Journal of Medicine and Public Health 72(Suppl. 2), 35–40.Google Scholar
Pascual, J. E., Bouli, R. P. and Aguiar, H. (1981). Eosinophilic meningoencephalitis in Cuba, caused by Angiostrongylus cantonensis . American Journal of Tropical Medicine and Hygiene 30, 960–962.CrossRefGoogle ScholarPubMed
Poulin, R. (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.CrossRefGoogle Scholar
Qvarnstrom, Y. J., Bishop, H. and da Silva, A. (2013). Detection of rat lungworm in intermediate, definitive and paratenic hosts obtained from environmental sources. Hawai'i Journal of Medicine and Public Health 72(Suppl. 2), 63–69.Google Scholar
Raccurt, C. P., Blaise, J. and Durette-Desset, M. C. (2003). Presence of Angiostrongylus cantonensis in Haiti. Tropical Medicine and International Health 8, 423–426.Google Scholar
Reiczigel, J. (2003). Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.Google Scholar
Robinson, B. A., Tolan, W. and Golding-Beecher, O. (1990). Childhood pica. Some aspects of the clinical profile in Manchester, Jamaica. West Indian Medical Journal 39, 20–26.Google Scholar
Robinson, R. D., Waugh, C. A., Todd, C. D., Lorenzo-Morales, J. and Lindo, J. F. (2013). Rat lungworm: an emerging zoonosis in Jamaica. Hawai'i Journal of Medicine and Public Health 72(Suppl. 2), 33 (Refereed Abstract).Google Scholar
Rosenberg, G., and Drumm, D. (2004). Interactive key to Jamaican land snails. http://data.acnatsci.org/jamaica/keyinfo.html.Google Scholar
Rosenberg, G. and Muratov, I. V. (2006). Status Report on the terrestrial mollusca of Jamaica. Proceedings of the Academy of Natural Sciences of Philadelphia 155, 117–161.Google Scholar
Rózsa, L., Reiczigel, J. and Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.Google Scholar
Slom, T. J., Cortese, M. M., Gerber, S. I., Jones, R. C., Holtz, T. H., Lopez, A. S., Zambrano, C. H., Sufit, R. L., Sakolvaree, Y., Chaicumpa, W., Herwaldt, B. L. and Johnson, S. (2002). An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. New England Journal of Medicine 346, 668–675.CrossRefGoogle ScholarPubMed
Spratt, D. M. (2015). Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. International Journal for Parasitology: Parasites and Wildlife 4, 178–189.Google Scholar
Thiengo, S. C., Simões Rde, O., Fernandez, M. A. and Maldonado, A. (2013). Angiostrongylus cantonensis and rat lungworm disease in Brazil. Hawaii Journal of Medicine and Public Health 72(Suppl. 2), 18–22.Google Scholar
Vargas, M., Gomez Perez, J. D. and Malek, E. A. (1992). First record of Angiostrongylus cantonensis (Chen, 1935) Nematoda: Metastrongylidae in the Dominican Republic. Tropical Medicine and Parasitology 43, 253–255.Google ScholarPubMed
Wallace, G. D. and Rosen, L. (1966). Studies on eosinophilic meningitis. 2. Experimental infection of shrimp and crabs with Angiostrongylus cantonensis . American Journal of Epidemiology 84, 120–131.Google Scholar
Waugh, C. A., Shafir, S., Wise, M., Robinson, R. D., Eberhard, M. and Lindo, J. F. (2005). Human Angiostrongylus cantonensis, Jamaica. Emerging Infectious Diseases 11, 1977–1978.Google Scholar
Waugh, C. A., Lindo, J. F., Forona, P., Angeles-Santana, M., Lorenzo-Morales, J. and Robinson, R. D. (2006). Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. Journal of Parasitology 92, 1014–1018.Google Scholar
Webster, J. P., Brunton, C. F. and MacDonald, D. W. (1994). Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus . Parasitology 109, 37–43.Google Scholar
Wilson, B. S. (1991). Latitudinal variation in activity season mortality rates of the lizard Uta stansburiana . Ecological Monographs 61, 393–414.Google Scholar
Wong, M. S., Bundy, D. A. and Golden, M. H. (1991). The rate of ingestion of Ascaris lumbricoides and Trichuris trichiura eggs in soil and its relationship to infection in two children's homes in Jamaica. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 89–91.Google Scholar
York, E. M., Butler, C. J. and Lord, W. D. (2014). Global decline in suitable habitat for Angiostrongylus (= Parastrongylus) cantonensis: the role of climate change. PLoS ONE 9, e103831.Google Scholar
Zhang, R.-L., Chen, M.-X., Gao, S.-T., Geng, Y.-J., Huang, D.-N., Liu, J.-P., Wu, Y.-L., and Zhu, X.-Q. (2008). Enzootic angiostrongyliasis in Shenzhen, China. Emerging Infectious Diseases 14, 1955–1956.Google Scholar