Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T13:22:09.744Z Has data issue: false hasContentIssue false
  • English
  • Français

Variation in Angiostrongylus cantonensis infection in definitive and intermediate hosts in Hawaii, a global hotspot of rat lungworm disease

Published online by Cambridge University Press:  10 September 2020

Chris N. Niebuhr Open the ORCID record for Chris N. Niebuhr [Opens in a new window] ,
Shane R. Siers ,
Israel L. Leinbach ,
Lisa M. Kaluna  and
Susan I. Jarvi Open the ORCID record for Susan I. Jarvi [Opens in a new window]
Chris N. Niebuhr*
Affiliation:
USDA APHIS Wildlife Services, National Wildlife Research Center, Hawaii Field Station, Hilo, HI, USA Manaaki Whenua–Landcare Research, PO Box 69040, Lincoln 7640, New Zealand
Shane R. Siers
Affiliation:
USDA APHIS Wildlife Services, National Wildlife Research Center, Hawaii Field Station, Hilo, HI, USA
Israel L. Leinbach
Affiliation:
USDA APHIS Wildlife Services, National Wildlife Research Center, Hawaii Field Station, Hilo, HI, USA
Lisa M. Kaluna
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
Susan I. Jarvi
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
*
Author for correspondence: Chris N. Niebuhr, E-mail: niebuhrc@landcareresearch.co.nz
Get access Rights & Permissions [Opens in a new window]

Abstract

Angiostrongylus cantonensis (rat lungworm) is a tropical and subtropical parasitic nematode, with infections in humans causing angiostrongyliasis (rat lungworm disease), characterized by eosinophilic meningitis. Hawaii has been identified as a global hotspot of infection, with recent reports of high infection rates in humans, as well as rat definitive and snail intermediate hosts. This study investigated variation in A. cantonensis infection, both prevalence and intensity, in wild populations of two species of rats (Rattus exulans and R. rattus) and one species of snail (Parmarion martensi). An overall infection prevalence of 86.2% was observed in P. martensi and 63.8% in rats, with R. exulans (77.4%) greater than R. rattus (47.6%). We found infections to vary with environmental and host-related factors. Body mass was a strong predictor of infection in all three species, with different patterns seen between sexes and species of rats. Infection prevalence and intensity for R. exulans were high in May 2018 and again in February 2019, but generally lower and more variable during the intervening months. Information on sources of variability of infection in wild host populations will be a crucial component in predicting the effectiveness of future disease surveillance or targeted management strategies.

Keywords

Angiostrongyliasisdriverseosinophilic meningitisnematodeparasiteParmarionRattusslugsnailtransmission
Type
Research Article
Information
Parasitology , Volume 148 , Special Issue 2: 6th International Workshop on Angiostrongylus and Angiostrongyliasis, Hilo, Hawai'i, USA, January, 2020 , February 2021 , pp. 133 - 142
Check for updates
Copyright
Copyright © The Author(s), 2020. This is a work of the U.S. Government and is not subject to copyright protection in the United States. Published by Cambridge University Press.

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

Alicata, JE (1991) The discovery of Angiostrongylus cantonensis as a cause of human eosinophilic meningitis. Parasitology Today 7, 151–153.CrossRefGoogle ScholarPubMed
Anderson, DR (2008) Model Based Inference in the Life Sciences: a Primer on Evidence. New York, New York, USA: Springer Science + Business Media, LLC.CrossRefGoogle 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 ScholarPubMed
Au, ACS and Ko, RC (1979) Changes in worm burden, haematological and serological response in rats after single and multiple Angiostrongylus cantonensis infections. Parasitology Research 58, 233–242.Google ScholarPubMed
Barratt, J, Chan, D, Sandaradura, I, Malik, R, Spielman, D, Lee, R, Marriott, D, Harkness, J, Ellis, J and Stark, D (2016) Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology 143, 1087–1118.CrossRefGoogle ScholarPubMed
Boss, KJ (1974) Oblomovism in the Mollusca. Transactions of the American Microscopical Society 93, 460–481.CrossRefGoogle ScholarPubMed
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach, 2nd Edn., New York, New York, USA: Springer-Verlag.Google Scholar
Bustin, SA, Benes, V, Garson, JA, Hellemans, J, Huggett, J, Kubista, M, Mueller, R, Nolan, T, Pfaffl, MW, Shipley, GL, Vandesompele, J and Wittwer, CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Červená, B, Modrý, D, Fecková, B, Hrazdilová, K, Foronda, P, Alonso, AM, Lee, R, Walker, J, Niebuhr, CN, Malik, R and Šlapeta, J (2019) Low diversity of Angiostrongylus cantonensis complete mitochondrial DNA sequences from Australia, Hawaii, French Polynesia and the Canary Islands revealed using whole genome next-generation sequencing. Parasites & Vectors 12, 241.CrossRefGoogle ScholarPubMed
Clark, D (1980) Age-and sex-dependent foraging strategies of a small mammalian omnivore. The Journal of Animal Ecology 49, 549–563.CrossRefGoogle Scholar
Cowie, RH (2013) Pathways for transmission of angiostrongyliasis and the risk of disease associated with them. Hawaii Journal of Medicine & Public Health 72, 70–74.Google Scholar
Gales, RP (1982) Age- and sex-related differences in diet selection by Rattus Rattus on Stewart Island, New Zealand. New Zealand Journal of Zoology 9, 463–466.CrossRefGoogle Scholar
Graeff-Teixeira, C, Da Silva, ACA and Yoshimura, K (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22, 322–348.CrossRefGoogle ScholarPubMed
Higa, HH, Brock, JA and Palumbo, NE (1986) Occurrence of Angiostrongylus cantonensis in rodents, intermediate and paratenic hosts on the island of Oahu. Journal of Environmental Health 48, 319–323.Google Scholar
Hirata, DN and Nass, RD (1974) Growth and sexual maturation of laboratory-reared, wild Rattus norvegicus, R. rattus, and R. exulans in Hawaii. Journal of Mammalogy 55, 472–474.CrossRefGoogle Scholar
Hollingsworth, RG, Kaneta, R, Sullivan, JJ, Bishop, HS, Qvarnstrom, Y, DaSilva, AJ and 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.CrossRefGoogle Scholar
Howe, K and Jarvi, SI (2017) Angiostrongyliasis (rat lungworm disease): viewpoints from Hawaii Island. ACS Chemical Neuroscience 8, 1820–1822.CrossRefGoogle Scholar
Howe, K, Kaluna, L, Fisher, BT, Tagami, Y and Mchugh, R (2019) Water transmission potential of Angiostrongylus cantonensis: larval viability and effectiveness of rainwater catchment sediment filters. PLoS ONE 14, e0209813.CrossRefGoogle ScholarPubMed
Ibrahim, MM (2007) Prevalence and intensity of Angiostrongylus cantonensis in freshwater snails in relation to some ecological and biological factors. Parasite 14, 61–70.CrossRefGoogle ScholarPubMed
Innes, JG (1990) Ship rat. In King, CM (ed.), The Handbook of New Zealand Mammals. Auckland, NZ: Oxford University Press, pp. 206–225.Google Scholar
Iskjaer, C, Slade, NA, Childs, JE, Glass, GE and Korch, GW (1989) Body mass as a measure of body size in small mammals. Journal of Mammalogy 70, 662–667.CrossRefGoogle Scholar
Jarvi, SI, Farias, MEM, Howe, K, Jacquier, S, Hollingsworth, R and Pitt, W (2012) Quantitative PCR estimates Angiostrongylus cantonensis (rat lungworm) infection levels in semi-slugs (Parmarion Martensi). Molecular and Biochemical Parasitology 185, 174–176.CrossRefGoogle Scholar
Jarvi, SI, Quarta, S, Jacquier, S, Howe, K, Bicakci, D, Dasalla, C, Lovesy, N, Snook, K, McHugh, R and Niebuhr, CN (2017) High prevalence of Angiostrongylus cantonensis (rat lungworm) on eastern Hawai'i Island: a closer look at life cycle traits and patterns of infection in wild rats (Rattus Spp.). PLoS ONE 12, e0189458.CrossRefGoogle Scholar
Jarvi, SI, Howe, K and Macomber, P (2018) Angiostrongyliasis or rat lungworm disease: a perspective from Hawai'i. Current Tropical Medicine Reports 5, 59–66.CrossRefGoogle Scholar
Ji, L, Yiyue, X, Xujin, H, Minghui, Z, Mengying, Z, Yue, H, Yanqi, W, Langui, S, Xin, Z, Datao, L, Shuo, W, Huanqin, Z, Zhongdao, W and Zhiyue, L (2017) Study on the tolerance and adaptation of rats to Angiostrongylus cantonensis infection. Parasitology Research 116, 1937–1945.CrossRefGoogle Scholar
Johnston, DI, Dixon, MC, Elm, JL, Calimlim, PS, Sciulli, RH and Park, SY (2019) Review of Cases of Angiostrongyliasis in Hawaii, 2007–2017. The American Journal of Tropical Medicine and Hygiene 101, 608–616.CrossRefGoogle ScholarPubMed
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, 21–26.Google ScholarPubMed
Kim, JR, Wong, TM, Curry, PA, Yeung, NW, Hayes, KA and Cowie, RH (2019) Modelling the distribution in Hawaii of Angiostrongylus cantonensis (rat lungworm) in its gastropod hosts. Parasitology 146, 42–49.CrossRefGoogle ScholarPubMed
Liat, LB, Kong, OC and Joe, LK (1965) Natural infection of Angiostrongylus cantonensis in Malaysian rodents and intermediate hosts and preliminary observations on acquired resistance. American Journal of Tropical Medicine and Hygiene 14, 610–621.CrossRefGoogle Scholar
Niebuhr, CN, Jarvi, SI and Siers, SR (2019) A review of rat lungworm infection and recent data on its definitive hosts in Hawaii. Human-Wildlife Interactions 13, 238–249.Google Scholar
Niebuhr, CN, Jarvi, SI, Kaluna, L, Fischer, BLT, Deane, AR, Leinbach, IL and Siers, SR (2020) Occurrence of rat lungworm (Angiostrongylus cantonensis) in invasive coqui frogs (Eleutherodactylus Coqui) and other hosts in Hawaii. Journal of Wildlife Diseases 56, 203–207.CrossRefGoogle ScholarPubMed
NNDC CDO (2020) NOAA National Data Center Climate Data Online. National Climatic Data Center, Asheville, NC, USA. Available at http://cdo.ncdc.noaa.gov/CDO/cdo (Accessed 15 April 2020).Google Scholar
Prociv, P, Spratt, DM and Carlisle, MS (2000) Neuro-angiostrongyliasis: unresolved issues. International Journal for Parasitology 30, 1295–1303.CrossRefGoogle ScholarPubMed
Qvarnstrom, Y, Bishop, HS and da Silva, AJ (2013) Detection of rat lungworm in intermediate, definitive, and paratenic hosts obtained from environmental sources. Hawaii Journal of Medicine & Public Health 72(suppl. 2), 63–69.Google ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Simões, RO, Maldonado Júnior, A, Olifiers, N, Garcia, JS, Bertolino, AVFA and Luque, JL (2014) A longitudinal study of Angiostrongylus cantonensis in an urban population of Rattus norvegicus in Brazil: the influences of seasonality and host features on the pattern of infection. Parasites & Vectors 7, 1–8.CrossRefGoogle Scholar
Spratt, DM (2015) Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. International Journal for Parasitology: Parasites and Wildlife 4, 178–189.Google ScholarPubMed
Sugihara, RT (1997) Abundance and diets of rats in two native Hawaiian forests. Pacific Science 51, 189–198.Google Scholar
Wang, QP, Lai, DH, Zhu, XQ, Chen, XG and Lun, ZR (2008) Human angiostrongyliasis. The Lancet Infectious Diseases 8, 621–630.CrossRefGoogle ScholarPubMed
Webster, JP and Macdonald, DW (1995) Parasites of wild brown rats (Rattus norvegicus) on UK farms. Parasitology 111, 247–255.CrossRefGoogle ScholarPubMed
Yong, WK and Dobson, CM (1982) The biology of Angiostrongylus cantonensis larvae in immune rats. Southeast Asian Journal of Tropical Medicine and Public Health 13, 244–248.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Supplementary material: File

Niebuhr et al. supplementary material

Tables S1-S3

Download Niebuhr et al. supplementary material(File)
File 18 KB