Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-22T14:52:37.611Z Has data issue: false hasContentIssue false
  • English
  • Français

Validation of a death assay for Angiostrongylus cantonensis larvae (L3) using propidium iodide in a rat model (Rattus norvegicus)

Published online by Cambridge University Press:  31 July 2019

Susan I. Jarvi Open the ORCID record for Susan I. Jarvi [Opens in a new window] ,
John Jacob ,
Robert T. Sugihara ,
Israel L. Leinbach ,
Ina H. Klasner ,
Lisa M. Kaluna ,
Kirsten A. Snook ,
M. Kathleen Howe ,
Steven H. Jacquier  and
Ingo Lange
...Show all authors
Susan I. Jarvi*
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
John Jacob
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
Robert T. Sugihara
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
Ina H. Klasner
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, 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
Kirsten A. Snook
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
M. Kathleen Howe
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
Steven H. Jacquier
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
Ingo Lange
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
Abigail L. Atkinson
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, Hilo, HI, USA
Ashley R. Deane
Affiliation:
Department of Psychology, University of Otago, Dunedin, New Zealand
Chris N. Niebuhr
Affiliation:
USDA APHIS Wildlife Services, National Wildlife Research Center, Hawaii Field Station, Hilo, HI, USA
Shane R. Siers
Affiliation:
USDA APHIS Wildlife Services, National Wildlife Research Center, Hawaii Field Station, Hilo, HI, USA
*
Author for correspondence: Susan I. Jarvi, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Angiostrongylus cantonensis is a pathogenic nematode and the cause of neuroangiostrongyliasis, an eosinophilic meningitis more commonly known as rat lungworm disease. Transmission is thought to be primarily due to ingestion of infective third stage larvae (L3) in gastropods, on produce, or in contaminated water. The gold standard to determine the effects of physical and chemical treatments on the infectivity of A. cantonensis L3 larvae is to infect rodents with treated L3 larvae and monitor for infection, but animal studies are laborious and expensive and also raise ethical concerns. This study demonstrates propidium iodide (PI) to be a reliable marker of parasite death and loss of infective potential without adversely affecting the development and future reproduction of live A. cantonensis larvae. PI staining allows evaluation of the efficacy of test substances in vitro, an improvement upon the use of lack of motility as an indicator of death. Some potential applications of this assay include determining the effectiveness of various anthelmintics, vegetable washes, electromagnetic radiation and other treatments intended to kill larvae in the prevention and treatment of neuroangiostrongyliasis.

Keywords

Angiostrongylus cantonensisautofluorescencenematodeneuroangiostrongyliasispropidium iodiderat lungwormvalidated death assay
Type
Research Article
Information
Parasitology , Volume 146 , Issue 11 , September 2019 , pp. 1421 - 1428
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

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

Anderson, RV, Gould, WD, Ingham, RE and Coleman, DC (1979) A staining method for nematodes: determination of nematode resistant stage and direct count from soil. Transactions of the American Microscopical Society American Microscopical Society 989, 213–218.Google Scholar
Ash, LR (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
Besselsen, DG (1995) Detection of rodent parvoviruses by PCR. In Meltzer, SJ (ed.) PCR in Bioanalysis. Methods in Molecular Biology, 92, 31–37. Humana Press, Inc, Totowa, NJ.Google Scholar
Chandel, ST (2002) Saffron stain for differentiating live and dead nematodes. Nematologia Mediterranea 30, 137–138.Google Scholar
Cheng, TC and Alicata, JE (1964) Possible role of water in the transmission of Angiostrongylus cantonensis (Nematoda: Metastrongylidae). Journal of Parasitology 50, 39–40.Google Scholar
Cox, GN, Staprans, S and Edgar, RS (1981) The cuticle of Caenorhabditis elegans: II. Stage-specific changes in ultrastructure and protein composition during postembryonic development. Developmental Biology 86, 456–470.Google Scholar
Croce, AC and Bottiroli, G (2014) Autofluorescence spectroscopy and imaging: a tool for biomedical research and diagnosis. European Journal of Histochemistry 58, 2461.Google Scholar
Crook, JR, Fulton, SE and Supanwong, K (1971) The infectivity of third stage Angiostrongylus cantonensis larvae shed from drowned Achatina fulica snail and the effect of chemical agents on infectivity. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 5.Google Scholar
Ferreira, SR, Mendes, TAO, Bueno, LL, de-Araújo, JV, Bartholomeu, DC and Fujiwara, RT (2015) A new methodology for evaluation of nematode viability. BioMed Research International, 1–7. doi.org/10.1155/2015/879263.Google Scholar
Gilbert, DL and Ehrenstein, G (1984) Membrane surface charge. Current Topics in Membrane Transport 22, 407–421.Google Scholar
Hammoud, RA, Nayes, SL, Murphy, JR, Heresi, GP, Butler, IJ and Pérez, N (2017) Angiostrongylus cantonensis Meningitis and myelitis, Texas, USA. Emerging Infectious Diseases 23, 1037–1038.Google Scholar
Heyneman, D and Lim, BL (1967) Angiostrongylus cantonensis: proof of direct transmission with its epidemiological implications. Science 158, 1057.Google Scholar
Hollingsworth, RG, Kaneta, R, Sullivan, JJ, Bishop, HS, Qvarnstrom, Y, da Silva, AJ and Robinson, DG. (2007) Distribution of Parmarion cf. Martensi (Pulmonata: Helicarionidae), a new semi-slug pest on Hawaii Island, and it's potential as a vector for human angiostrongyliasis. Pacific Science 61, 457–467.Google Scholar
Howe, K and Jarvi, SJ (2017) Angiostrongyliasis (rat lungworm disease): viewpoints from Hawai`i Island. ACS Chemical Neuroscience 8, 1820–1822.Google Scholar
Howe, K, Kaluna, L, Lozano, A, Torres Fischer, B, Tagami, Y, McHugh, R and Jarvi, S (2019) Water transmission potential of Angiostrongylus cantonensis: larval viability and effectiveness of rainwater catchment sediment filters. PLoS ONE 14, e0209813. https://doi.org/10.1371/journal.pone.0209813.Google Scholar
Jarvi, SI, Farias, ME, Howe, K, Jacquier, S, Hollingsworth, R and Pitt, W (2012) Quantitative PCR estimates Angiostrongylus cantonensis infection levels in semi-slugs (Parmarion martensi). Molecular and Biochemical Parasitology 185, 174–176.Google Scholar
Jarvi, SI, Howe, K and Macomber, P (2018) Angiostrongyliasis or rat lungworm disease: a perspective from Hawai'i. Current Tropical Medicine Reports. https://doi.org/10.1007/s40475-018-0132-z.Google 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. https://doi.org/10.1371/journal.pone.0189458.Google Scholar
Kim, JR, Wong, TM, Curry, PA, Yeung, NW, Hayes, KA and Cowie, RH (2018) Modelling the distribution in Hawaii of Angiostrongylus cantonensis (rat lungworm) in its gastropod hosts. Parasitology 146, 42–49.Google Scholar
Kusnawidjaja, K (1960) Vital stains acridine orange, mercurochrome, Nile blue and Victoria blue for nematodes. Madjalah Kedokt Indones 10, 434–439.Google Scholar
Lv, S, Zhang, Y, Zhang, C, Steinmann, P, Zhou, X and Utzinger, J (2009) Angiostrongylus cantonensis: morphological and behavioral investigation within the freshwater snail Pomacea canaliculata. Parasitology Research 104, 1351–1359.Google Scholar
Mackerras, MJ and Sandars, DF (1955) The life history of the rat lung-worm, Angiostrongylus cantonensis (Chen) (Nematoda: Metastrongylidae). Australian Journal of Zoology 3, 1–25.Google Scholar
Matute, MM (2013) Soil nematodes of Brassica rapa: influence of temperature and pH. Advances in Natural Science 6, 20–26.Google Scholar
Mentz, MB and Graeff-Teixeira, C (2003) Drug trials for treatment of human Angiostrongyliasis (review). Journal of the São Paulo Institute of Tropical Medicine 45, 179–184.Google Scholar
Minitab Inc. (2010) Minitab 18 Statistical Software (2010). State College, PA, USA: Minitab, INc. (www.minitab.com).Google Scholar
Page, AP, Stepek, G, Winter, AD and Pertab, D (2014) Enzymology of the nematode cuticle: a potential drug target? International Journal for Parasitology: Drugs and Drug Resistance 4, 133–141.Google Scholar
Paxinos, G and Watson, C (2007) The Rat Brain in Stereotaxic Coordinates, 6th Edn. New York: Elsevier/Academic Press.Google Scholar
Prince, AM and Andrus, L (1992) PCR: how to kill unwanted DNA. Biotechniques 12, 358–359.Google Scholar
Richards, CS and Merritt, JW (1967) Studies on Angiostrongylus cantonensis molluscan intermediates hosts. Journal of Parasitology 53, 382–388.Google Scholar
Sano, M, Terada, M, Ishii, A, Kino, H and Hayashi, M (1981) Studies on chemotherapy of parasitic helminths. (I). On the in vitro methods and paralyzing effects of avermectin B1a on Angiostrongylus cantonensis. Japanese Journal Parasitology 30, 305–314.Google Scholar
Sikes, RS, Gannon, WL and The animal care and use committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammologists for the use of wild mammals in research. Journal of Mammalogy 92, 235–253.Google Scholar
Stockdale Walden, HD, Slapcinsky, JD, Roff, S, Mendieta Calle, J, Diaz Goodwin, Z and Stern, J (2017) Geographic distribution of Angiostrongylus cantonensis in wild rats (Rattus rattus) and terrestrial snails in Florida, USA. PLoS ONE 12, e0177910.Google Scholar
Teem, JL, Qvarnstrom, Y, Bishop, HS, Alexandre, JD, Carter, J, White-Mclean, J and Smith, T (2013) The occurrence of the rat lungworm, Angiostrongylus cantonensis, in nonindigenous snails in the Gulf of Mexico region of the United States. Hawai'i Journal of Medicine & Public Health 72(6 suppl. 2), 11–14.Google Scholar
Terada, M, Rodriguez, BO, Dharejo, AM, Ishii, AI and Sano, M (1986) Study of chemotherapy of parasitic helminthes (XXVI). comparative in-vitro effects of various anthelmintics on the motility of Angiostrongylus costaricensis and A. cantonensis. Japanese Journal of Parasitology 35, 365–367.Google Scholar
Wang, LC, Chao, D and Chen, ER (1991) Experimental infection routes of Angiostrongylus cantonensis in mice. Journal of Helminthology 65, 296–300.Google Scholar
Wang, QP, Lai, DH, Zhu, XQ, Chen, XG and Lun, ZR (2008) Human angiostrongyliasis. The Lancet Infectious Diseases 8, 621–630.Google Scholar
Wharton, DA (1986) Life cycle. In Carlow, P (ed.) A Functional Biology of Nematodes. Functional Biology Series. Boston, MA: Springer. doi.org/10.1007/978-1-4615-8516-9_6.Google Scholar
Zanini, GM and Graeff-Teixeira, C (2001) Inactivation of infective larvae of Angiostrongylus costaricensis with short time incubations in 1.5% bleach solution, vinegar or saturated cooking salt solution. Acta Tropica 78, 17–21.Google Scholar
Zhao, H, Oczos, J, Janowski, P, Trembecka, D, Dobrucki, J, Darzynkiewicz, Z and Wlodkowic, D (2010) Rationale for the real-time and dynamic cell death assays using propidium iodide. Cytometry Part A 77, 399–405.Google Scholar