Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-23T14:27:04.442Z Has data issue: false hasContentIssue false
  • English
  • Français

Modelling the distribution in Hawaii of Angiostrongylus cantonensis (rat lungworm) in its gastropod hosts

Published online by Cambridge University Press:  21 June 2018

Jaynee R. Kim ,
Tamara M. Wong ,
Patrick A. Curry ,
Norine W. Yeung ,
Kenneth A. Hayes  and
Robert H. Cowie Open the ORCID record for Robert H. Cowie [Opens in a new window]
Jaynee R. Kim
Affiliation:
Department of Biology, University of Hawaii, 2538 McCarthy Mall, Honolulu, Hawaii 96822, USA Pacific Biosciences Research Center, University of Hawaii, 3050 Maile Way, Honolulu, Hawaii 96822, USA
Tamara M. Wong
Affiliation:
Department of Botany, University of Hawaii, 3190 Maile Way, Honolulu, Hawaii 96822, USA
Patrick A. Curry
Affiliation:
Pacific Biosciences Research Center, University of Hawaii, 3050 Maile Way, Honolulu, Hawaii 96822, USA
Norine W. Yeung
Affiliation:
Pacific Biosciences Research Center, University of Hawaii, 3050 Maile Way, Honolulu, Hawaii 96822, USA Bishop Museum, 1525 Bernice Street, Honolulu, Hawaii 96817, USA
Kenneth A. Hayes
Affiliation:
Bishop Museum, 1525 Bernice Street, Honolulu, Hawaii 96817, USA
Robert H. Cowie
Affiliation:
Pacific Biosciences Research Center, University of Hawaii, 3050 Maile Way, Honolulu, Hawaii 96822, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

Angiostrongylus cantonensis (rat lungworm), a parasitic nematode, is expanding its distribution. Human infection, known as angiostrongyliasis, may manifest as eosinophilic meningitis, an emerging infectious disease. The range and incidence of this disease are expanding throughout the tropics and subtropics. Recently, the Hawaiian Islands have experienced an increase in reported cases. This study addresses factors affecting the parasite's distribution and projects its potential future distribution, using Hawaii as a model for its global expansion. Specimens of 37 snail species from the Hawaiian Islands were screened for the parasite using PCR. It was present on five of the six largest islands. The data were used to generate habitat suitability models for A. cantonensis, based on temperature and precipitation, to predict its potential further spread within the archipelago. The best current climate model predicted suitable habitat on all islands, with greater suitability in regions with higher precipitation and temperatures. Projections under climate change (to 2100) indicated increased suitability in regions with estimated increased precipitation and temperatures, suitable habitat occurring increasingly at higher elevations. Analogously, climate change could facilitate the spread of A. cantonensis from its current tropical/subtropical range into more temperate regions of the world, as is beginning to be seen in the continental USA.

Keywords

Angiostrongylusclimateemerging infectious diseasehabitat suitabilityinvasive speciesnematoderat lungwormsnails
Type
Research Article
Information
Parasitology , Volume 146 , Issue 1 , January 2019 , pp. 42 - 49
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agresti, A (1996) An Introduction to Categorical Data Analysis. New York: Wiley.Google Scholar
Alicata, JE (1965) Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. Advances in Parasitology 3, 223–248.Google Scholar
Amarasekare, P (1994) Ecology of introduced small mammals on western Mauna Kea, Hawaii. Journal of Mammalogy 75, 24–38.Google Scholar
Ash, LR (1962) The helminth parasites of rats in Hawaii and the description of Capillaria traverae sp. n. Journal of Parasitology 48, 66–68.Google Scholar
Beaver, PC and Rosen, L (1964) Memorandum on the first report of Angiostrongylus in man by Nomura and Lin, 1945. American Journal of Tropical Medicine and Hygiene 13, 589–590.Google Scholar
Bergey, EA, Figueroa, LL, Mather, CM, Martin, RJ, Ray, EJ, Kurien, JT, Westrop, DR and Suriyawong, P (2014) Trading in snails and slugs: plant nurseries as transport hubs for non-native species. Biological Invasions 16, 1441–1451.Google Scholar
Burns, RE, Bicknese, EJ, Qvarnstrom, Y, DeLeon-Carnes, M, Drew, CP, Gardiner, CH and Rideout, BA (2014) Cerebral Angiostrongylus cantonensis infection in a captive African pygmy falcon (Polihierax semitorquatus) in southern California. Journal of Veterinary Diagnostic Investigation 26, 695–698.Google Scholar
Calcagno, V (2013) Glmulti: model selection and multimodel inference made easy. R package version 1.0.7. Available at: http://cran.r-project.org/web/packages/glmulti/index.html.Google Scholar
Collins, M, Knutti, R, Arblaster, J, Dufresne, J-L, Fichefet, T, Friedlingstein, P, Gao, X, Gutowski, WJ, Johns, T, Krinner, G, Shongwe, M, Tebaldi, C, Weaver, AJ and Wehner, M (2013) Long-term climate change: projections, commitments and irreversibility. In Stocker, TF, Qin, D, Plattner, G-K, Tignor, M, Allen, SK, Boschung, J, Nauels, A, Xia, Y, Bex, V and Midgley, PM (eds), Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press, pp. 1029–1136.Google Scholar
Cowie, RH (2013 a) Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawaii Journal of Medicine and Public Health 72(Suppl. 2), 6–9.Google Scholar
Cowie, RH (2013 b) Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawaii Journal of Medicine and Public Health 72(Suppl. 2), 70–74.Google Scholar
Cowie, RH (2017) Angiostrongylus cantonensis: agent of a sometimes fatal globally emerging infectious disease (rat lungworm disease). ACS Chemical Neuroscience 8, 2102–2104.Google Scholar
Cowie, RH and Robinson, DG (2003) Pathways of introduction of nonindigenous land and freshwater snails and slugs. In Ruiz, G and Carlton, JT (eds), Invasive Species: Vectors and Management Strategies. Washington, DC: Island Press, pp. 93–122.Google Scholar
Cowie, RH, Hayes, KA, Tran, CT and Meyer, WM III (2008) The horticultural industry as a vector of alien snails and slugs: widespread invasions in Hawaii. International Journal of Pest Management 54, 267–276.Google Scholar
Cowie, RH, Hayes, KA, Kim, JR, Bustamente, KM and Yeung, NW (2018) Parmarion martensi Simroth, 1893 (Gastropoda: Ariophantidae), an intermediate host of Angiostrongylus cantonensis (rat lungworm), on Maui. Bishop Museum Occasional Papers 123, 7–10.Google Scholar
Crase, B, Vesk, PA, Liedloff, A and Brendan, WA (2015) Modelling both dominance and species distribution provides a more complete picture of changes to mangrove ecosystems under climate change. Global Change Biology 21, 3005–3020.Google Scholar
Crawley, MJ (2007) The R Book. Chichester: Wiley.Google Scholar
De'ath, G (2007) Boosted trees for ecological modeling and prediction. Ecology 88, 243–251.Google Scholar
Elith, J and Leathwick, JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40, 677–697.Google Scholar
Elith, J, Leathwick, JR and Hastie, T (2008) A working guide to boosted regression trees. Journal of Animal Ecology 77, 802–813.Google Scholar
Flerlage, T, Qvarnstrom, Y, Noh, J, Devicenzo, JP, Madni, A, Bagga, B and Hysmith, ND (2017) Angiostrongylus cantonensis eosinophilic meningitis in an infant, Tennessee, USA. Emerging Infectious Diseases 23, 1756–1758.Google Scholar
Gaston, KJ (2003) The Structure and Dynamics of Geographic Ranges. Oxford: Oxford University Press.Google Scholar
Giambelluca, TW, Chen, Q, Frazier, AG, Price, JP, Chen, Y-L, Chu, P-S, Eischeid, JK and Delparte, DM (2013) Online rainfall atlas of Hawaii. Bulletin of the American Meteorological Society 94, 313–316. http://rainfall.geography.hawaii.edu.Google Scholar
Giambelluca, TW, Shuai, X, Barnes, ML, Alliss, RJ, Longman, RJ, Miura, T, Chen, Q, Frazier, AG, Mudd, RG, Cuo, L and Businger, AD (2014) Evapotranspiration of Hawai'i. Final report submitted to the U.S. Army Corps of Engineers – Honolulu District, and the Commission on Water Resource Management, State of Hawai'i. http://climate.geography.hawaii.edu/.Google Scholar
Guisan, A and Zimmermann, NE (2000) Predictive habitat distribution models in ecology. Ecological Modelling 135, 147–186.Google Scholar
Haak, D (2015) Bioenergetics and habitat suitability models for the Chinese mystery snail (Bellamya chinensis). PhD dissertation, University of Nebraska.Google Scholar
Hijmans, RJ, van Etten, J, Cheng, J, Mattiuzzi, M, Sumner, M, Greenberg, JA, Lamigueiro, OP, Bevan, A, Racine, EB, Shortridge, A and Hijmans, MR (2015) Package ‘raster’: geographic data analysis and modeling. Available at: http://cran.r-project.org/package=raster.Google Scholar
Hochberg, NS, Park, SY, Blackburn, BG, Sejvar, JJ, Gaynor, K, Chung, H, Leniek, K, Herwaldt, BL and Effler, PV (2007) Distribution of eosinophilic meningitis cases attributable to Angiostrongylus cantonensis, Hawaii. Emerging Infectious Diseases 13, 1675–1680.Google Scholar
Horio, SR and Alicata, JE (1961). Parasitic meningo-encephalitis in Hawaii. A new parasitic disease of man. Hawaii Medical Journal 21, 139–140.Google Scholar
Howe, K and Jarvi, SI (2017) Angiostrongyliasis (rat lungworm disease): viewpoints from Hawai'i island. ACS Chemical Neuroscience 8, 1820–1822.Google Scholar
Jump, AS, Mátyás, C and Peñuelas, J (2009) The altitude-for-latitude disparity in the range retractions of woody species. Trends in Ecology and Evolution 24, 694–701.Google Scholar
Kim, JR, Hayes, KA, Yeung, NW and Cowie, RH (2014) Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLoS ONE 9(5), e94969.Google Scholar
LeDell, E, Petersen, M and van der Laan, M (2013) Package cvAUC: Cross-validated area under the ROC curve confidence intervals. Available at: ftp://ftp.sam.math.ethz.ch/sfs/Software/R-CRAN/web/packages/cvAUC/cvAUC.pdf.Google Scholar
Lu, HHS, Schölkopf, B and Zhao, H (2011) Handbook of Statistical Bioinformatics. New York: Springer.Google Scholar
Lv, S, Zho, XN, Zhang, Y, Liu, HX, Zhu, D, Yin, WG, Steinmann, P, Wang, XH and Jia, TW (2006) The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822). Parasitology Research 99, 583–587.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
Manning, C (2007) Logistic Regression (with R). http://nlp.stanford.edu/manning/courses/ling289/logistic.pdf (Accessed 6 November 2017).Google Scholar
Nakicenovic, N and Swart, R (2000) Emission Scenarios. Cambridge: Cambridge University Press.Google Scholar
Qvarnstrom, Y, Sullivan, JJ, Bishop, HS, Hollingsworth, R and da Silva, AJ (2007) PCR-based detection of Angiostrongylus cantonensis in tissue and mucus secretions from molluscan hosts. Applied and Environmental Microbiology 73, 1415–1419.Google Scholar
Qvarnstrom, Y, da Silva, ACA, Teem, JL, Hollingsworth, R, Bishop, H, Graeff-Teixeira, C and da Silva, AJ (2010) Improved molecular detection of Angiostrongylus cantonensis in mollusks and other environmental samples with a species-specific internal transcribed spacer 1-based TaqMan assay. Applied and Environmental Microbiology 76, 5287–5289.Google Scholar
Richards, CS and Merritt, JW (1967) Studies on Angiostrongylus cantonensis in molluscan intermediate hosts. Journal of Parasitology 53, 382–388.Google Scholar
Ridgeway, G. (2015) gbm: Generalized boosted regression models. Available at: http://CRAN.R-project.org/package=gbm.Google Scholar
Rosen, L, Laigret, J and Bories, S (1961) Observations on an outbreak of eosinophilic meningitis on Tahiti, French Polynesia. American Journal of Hygiene 74, 26–42.Google Scholar
Schröder, W and Schmidt, G (2014) Modelling Potential Malaria Spread in Germany by use of Climate Change Projections. A Risk Assessment Approach Coupling Epidemiologic and Geostatistical Measures. SpringerBriefs in Environmental Science. Heidelberg: Springer International Publishing. doi: 10.1007/978-3-319-03823-0.Google Scholar
Stockdale Walden, HD, Slapcinsky, JD, Roff, S, Calle, JM, Goodwin, ZD, Stern, J, Corlett, R, Conway, J and McIntosh, A (2017) Geographic distribution of Angiostrongylus cantonensis in wild rats (Rattus rattus) and terrestrial snails in Florida, USA. PLoS ONE 12(5), e0177910.Google Scholar
Swets, JA (1988) Measuring the accuracy of diagnostic systems. Science 240, 1285–1293.Google Scholar
Wang, QP, Lai, DH, Zhu, XQ, Chen, XG and Lun, ZR (2008) Human angiostrongyliasis. Lancet Infectious Diseases 8, 621–630.Google Scholar
Yong, HS and Eamsobhana, P (2015) Definitive rodent hosts of the rat lungworm Angiostrongylus cantonensis. Raffles Bulletin of Zoology Suppl. 29, 111–115.Google Scholar
York, EM, Butler, CJ and Lord, WD (2014) Global decline in suitable habitat for Angiostrongylus (=Parastrongylus) cantonensis: the role of climate change. PLoS ONE 9(8), e103831.Google Scholar
York, EM, Creecy, JP, Lord, WD and Caire, W (2015) Geographic range expansion for the rat lungworm in North America. Emerging Infectious Diseases 21, 1234–1236.Google Scholar
Zhang, CX, Wang, Y, Lauer, A and Hamilton, K (2012). Configuration and evaluation of the WRF model for the study of Hawaiian regional climate. Monthly Weather Review 140, 3259–3277.Google Scholar
Supplementary material: PDF

Kim et al. supplementary material 1

Kim et al. supplementary material

Download Kim et al. supplementary material 1(PDF)
PDF 3.2 MB