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Species Identity and Size are Associated with Rat Lungworm Infection in Gastropods

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Abstract

Angiostrongylus cantonensis, the rat lungworm, is an emerging zoonotic pathogen that cycles between definitive rat and intermediate gastropod hosts. Zoonotic infection occurs when humans intentionally or accidentally consume infectious larvae in a gastropod host, and may manifest as neuroangiostrongyliasis, characterized by eosinophilic meningitis, severe neurological impairment, and even death. Thus, the risk of A. cantonensis zoonoses may be related to the distribution of A. cantonensis larvae across gastropod hosts. We screened 16 gastropod species from 14 communities on the island of O‘ahu, Hawai‘i, USA, to characterize the distribution of A. cantonensis among species and across host size. Prevalence (proportion of the population infected) and infection intensity (density of worms in host tissue) varied among gastropod species. Prevalence also varied with gastropod host size, but this relationship differed among host species. Most host species showed a positive increase in the probability of infection with host size, suggesting that within species relatively larger hosts had higher prevalence. The density of worms in an infected snail was unrelated to host size. These results suggest that variation in A. cantonensis infection is associated with demographic structure and composition of gastropod communities, which could underlie heterogeneity in the risk of human angiostrongyliasis across landscapes.

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References

  • Alicata JE (1964) Parasitic Infections of Man and Animals in Hawaii. Technical Bulletin 61, Honolulu: Hawaii Agricultural Experiment Station, College of Tropical Agriculture, University of Hawaii

    Google Scholar 

  • Alicata JE, Jindrak K (1970) Angiostrongylosis in the Pacific and Southeast Asia, Springfield, IL: Charles C. Thomas Publisher

    Google Scholar 

  • Allan BF, Langerhans RB, Ryberg WA, Landesman WJ, Griffin NW, Katz RS, Oberle BJ, Schutzenhofer MR, Smyth KN, de St. Maurice A, Clark L, Crooks KR, Hernandez DE, McLean RG, Ostfeld RS, Chase JM (2009) Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158:699–708

    PubMed  Google Scholar 

  • Anderson DR, Burnham KP (2002) Avoiding pitfalls when using information-theoretic methods. Journal of Wildlife Management 66:912–918

    Google Scholar 

  • Barratt J, Chan D, Sandaradura I, Malik R, Spielman D, Lee R, Marriott D, Harkness J, Ellis J, Stark D (2016) Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology 143:1087–1118

    PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48

    Google Scholar 

  • Campbell BG, Little MD (1988) The finding of Angiostrongylus cantonensis in rats in New Orleans. American Journal of Tropical Medicine and Hygiene 38:568–573

    CAS  PubMed  Google Scholar 

  • Chen D, Zhang Y, Shen H, Wei Y, Huang D, Tan Q, Lan X, Li Q, Chen Z, Li Z, Ou L, Suen H, Ding X, Luo X, Li X, Zhan X (2011) Epidemiological survey of Angiostrongylus cantonensis in the west-central region of Guangdong Province, China. Parasitology Research 109:305–314

    PubMed  Google Scholar 

  • Combes C (1991) Evolution of parasite life cycles. In: Parasite-Host Associations: Coexistence or Conflict? Toft CA, Aeschlimann A, Bolis L (editors), Oxford: Oxford University Press, pp 62–82

    Google Scholar 

  • Cowie RH (1998) Patterns of introduction of non-indigenous non-marine snails and slugs in the Hawaiian Islands. Biodiversity and Conservation 7:349–368

    Google Scholar 

  • Cowie RH (2013) Biology, systematics, life cycle, and distribution of Angiostrongylus cantonensis, the cause of rat lungworm disease. Hawai‘i Journal of Medicine and Public Health 72(6 Supplement 2):6–9

    PubMed  Google Scholar 

  • Cowie RH (2013) Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawai‘i Journal of Medicine and Public Health 72(6 Supplement 2):70–74

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Cowie RH, Hayes KA, Tran CT, 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, Rollins RL, Medeiros MCI, Christensen CC (2019) New records of Clausiliidae: Tauphaedusa tau (Boettger, 1877) (Gastropoda: Heterobranchia) on O‘ahu, Hawaiian Islands, and the first global record of infection of a clausiliid land snail with Angiostrongylus cantonensis (Chen, 1935), the rat lungworm. Bishop Museum Occasional Papers 126:11–18

    Google Scholar 

  • Eamsobhana P, Yoolek A, Yong H-S (2010) Effect of Thai ‘koi-hoi’ food flavoring on the viability and infectivity of the third-stage larvae of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae). Acta Tropica 113:245–247

    PubMed  Google Scholar 

  • Fieberg J, Johnson DH (2015) MMI: multimodel inference or models with management implications? Journal of Wildlife Management 79:708–718

    Google Scholar 

  • Fukuda H, Haga T, Tatara Y (2008) Niku-nuki: a useful method for anatomical and DNA studies on shell-bearing molluscs. Zoosymposia 1:15–38

    Google Scholar 

  • Graeff Teixeira C, Thiengo SC, Thome JW, Medeiros AB, Camillo-Coura L, Agostini AA (1993) On the diversity of mollusc intermediate hosts of Angiostrongylus costaricensis Morera & Cespedes, 1971, in southern Brazil. Memórias do Instituto Oswaldo Cruz 8:487–489

    Google Scholar 

  • Graeff-Teixeira C, Goulart AH, de Ornellas Brum C, Laitano AC, Sievers-Tostes C, Zanini GM, Bered PL, Morassutti A, Geiger S, Abrahms-Sandi E, dos Santos Oliveira FT, Maurer RL, Aguiar LF, Garrido CT, da Silva ACA, Rodriguez R, Schulz-Key H, Agostini AA (2005) Longitudinal clinical and serological survey of abdominal angiostrongyliasis in Guaporé, southern Brazil, from 1995 to 1999. Revista da Sociedade Brasileira de Medicina Tropical 38:310–315

    PubMed  Google Scholar 

  • Graeff-Teixeira C, da Silva ACA, Yoshimura K (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22:322–348

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hamer GL, Chaves LF, Anderson TK, Kitron UD, Brawn JD, Ruiz MO, Loss SR, Walker ED, Goldberg TL (2011) Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission. PloS One 6(8):e23767

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hollingsworth RG, Kaneta R, Sullivan JJ, Bishop HS, Qvarnstrom Y, da Silva AJ, Robinson DG (2007) Distribution of Parmarion cf. martensi (Pulmonata: Helicarionidae), a new semi-slug pest on Hawai‘i Island, and its potential as a vector for human angiostrongyliasis. Pacific Science 61:457–467

    Google Scholar 

  • Horio SR, Alicata JE (1961) Parasitic meningo-encephalitis in Hawaii. A new parasitic disease of man. Hawaii Medical Journal 21:139–140

    CAS  PubMed  Google Scholar 

  • Ibrahim MM (2007) Prevalence and intensity of Angiostrongylus cantonensis in freshwater snails in relation to some ecological and biological factors. Parasite 14:61–70

    CAS  PubMed  Google Scholar 

  • Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD (2006) Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society of London B: Biological Sciences 273:2327–2333

    Google Scholar 

  • Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P (2006) West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biology 4(4):e82

    PubMed  PubMed Central  Google Scholar 

  • Kim JR, Hayes KA, Yeung NW, 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

    PubMed  PubMed Central  Google Scholar 

  • Kim JR, Wong TW, Curry PA, Yeung NW, Hayes KA, Cowie RH (2019) Modelling the distribution in Hawaii of Angiostrongylus cantonensis (rat lungworm) in its gastropod hosts. Parasitology 146:42–49

    PubMed  Google Scholar 

  • LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences of the United States of America 100:567–571

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lv S, Zhang Y, Chen S-R, Wang L-B, Fang W, Chen F, Jiang J-J, Li Y-L, Du Z-W, Zhou X-N (2009) Human angiostrongyliasis outbreak in Dali, China. PLoS Neglected Tropical Diseases 3(9):e520

    PubMed  PubMed Central  Google Scholar 

  • Lv S, Zhang Y, Steinmann P, Yang G-J, Yang K, Zhou X-N, 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 

  • Meyer WM III, Yeung NW, Slapcinsky J, Hayes KA (2017) Two for one: inadvertent introduction of Euglandina species during failed bio-control efforts in Hawaii. Biological Invasions 19:1399–1405

    Google Scholar 

  • Murphy GS, 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(6 Supplement 2):35–40

    PubMed  Google Scholar 

  • Oliveira APM, Gentile R, Maldonado A Jr, Torres EJL, Thiengo SC (2015) Angiostrongylus cantonensis infection in molluscs in the municipality of São Gonçalo, a metropolitan area of Rio de Janeiro, Brazil: role of the invasive species Achatina fulica in parasite transmission dynamics. Memórias do Instituto Oswaldo Cruz 110:739–744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prociv T, Turner M (2018) Neuroangiostrongyliasis: the “subarachnoid phase” and its implications for anthelminthic therapy. American Journal of Tropical Medicine and Hygiene 98:353–359

    PubMed  Google Scholar 

  • Qvarnstrom Y, da Silva ACA, Teem JL, Hollingsworth R, Bishop H, Graeff-Teixeira C, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slom TJ, Cortese MM, Gerber SI, Jones RC, Holtz TH, Lopez AS, Zambrano CH, Sufit RL, Sakolvaree Y, Chaicumpa W, Herwaldt BL, 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

    PubMed  Google Scholar 

  • Stockdale-Walden HD, Slapcinsky J, Qvarnstrom Y, McIntosh A, Bishop HS, Rosseland B (2015) Angiostrongylus cantonensis in introduced gastropods in southern Florida. Journal of Parasitology 101:156–159

    PubMed  Google Scholar 

  • Stockdale-Walden HD, Slapcinsky JD, Roff S, Calle JM, Goodwin ZD, Stern J, Corlett R, Conway J, McIntosh A (2017) Geographic distribution of Angiostrongylus cantonensis in wild rats (Rattus rattus) and terrestrial snails in Florida, USA. PLoS One 12(5):e0177910

    PubMed  PubMed Central  Google Scholar 

  • Taylor LH, Latham SM, Mark EJ (2001) Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London B: Biological Sciences 356:983–989

    CAS  PubMed  Google Scholar 

  • Tesana S, Srisawangwong T, Sithithaworn P, Laha T, Andrews R (2009) Prevalence and intensity of infection with third stage larvae of Angiostrongylus cantonensis in mollusks from northeast Thailand. American Journal of Tropical Medicine and Hygiene 80:983–987

    PubMed  Google Scholar 

  • Tsai H-C, Liu Y-C, Kunin CM, Lee SS-J, Chen Y-S, Lin H-H, Tsai T-H, Lin W-R, Huang C-K, Yen M-Y, Yen C-M (2001) Eosinophilic meningitis caused by Angiostrongylus cantonensis: report of 17 cases. American Journal of Medicine 111:109–114

    CAS  PubMed  Google Scholar 

  • Tsai H-C, Lee SS-J, Huang C-K, Yen C-M, Chen E-R, Liu Y-C (2004) Outbreak of eosinophilic meningitis associated with drinking raw vegetable juice in southern Taiwan. American Journal of Tropical Medicine and Hygiene 71:222–226

    PubMed  Google Scholar 

  • Wallace GD, Rosen L (1969) Studies on eosinophilic meningitis V. Molluscan hosts of Angiostrongylus cantonensis on Pacific islands. American Journal of Tropical Medicine and Hygiene 18:206–216

    CAS  PubMed  Google Scholar 

  • Waugh CA, Lindo JF, Lorenzo-Morales J, Robinson RD (2016) An epidemiological study of A. cantonensis in Jamaica subsequent to an outbreak of human cases of eosinophilic meningitis in 2000. Parasitology 143:1211–1217

    CAS  PubMed  Google Scholar 

  • Yeung NW, Hayes KA, Cowie RH (2013) Effects of washing produce contaminated with the snail and slug hosts of Angiostrongylus cantonensis with three common household solutions. Hawai‘i Journal of Medicine and Public Health 72(6 Supplement 2):83–86

    PubMed  Google Scholar 

  • York EM, Creecy JP, Lord WD, Caire W (2015) Geographic range expansion for the rat lungworm in North America. Emerging Infectious Diseases 21:1234–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yousif F, Lämmler G (1975) The effect of some biological and physical factors on infection of Biomphalaria glabrata with Angiostrongylus cantonensis. Zeitschrift für Parasitenkunde 47:191–201

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the numerous private landowners on O‘ahu who granted access to their land. Nicole Yoneishi assisted with screening gastropod hosts. Ken Hayes confirmed the correct name for the Meghimatium species. The study was funded in part by a grant (PI: Cowie) from the Hawai‘i Department of Health to train personnel and augment capacity across State of Hawai‘i institutions, and a National Science Foundation REU-Site award (NSF DBI 1659889). Publication number SOEST-no. 11094 of the University of Hawai‘i School of Ocean and Earth Science and Technology. Two anonymous reviewers improved an early version of this manuscript.

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Correspondence to Matthew C. I. Medeiros.

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Medeiros, M.C.I., Rollins, R.L., Echaluse, M.V. et al. Species Identity and Size are Associated with Rat Lungworm Infection in Gastropods. EcoHealth 17, 183–193 (2020). https://doi.org/10.1007/s10393-020-01484-x

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