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In vitro efficacy of anthelmintics on Angiostrongylus cantonensis L3 larvae

Published online by Cambridge University Press:  17 August 2020

John Jacob
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, The University of Hawai‘i at Hilo, Hawai‘i96720, USA
Ghee Tan
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, The University of Hawai‘i at Hilo, Hawai‘i96720, USA
Ingo Lange
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, The University of Hawai‘i at Hilo, Hawai‘i96720, USA
Hiwa Saeed
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, The University of Hawai‘i at Hilo, Hawai‘i96720, USA
Abhijit Date
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, The University of Hawai‘i at Hilo, Hawai‘i96720, USA
Susan Jarvi*
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, The University of Hawai‘i at Hilo, Hawai‘i96720, USA
*
Author for correspondence: Susan Jarvi, E-mail: [email protected]

Abstract

Angiostrongylus cantonensis is the leading cause of eosinophilic meningitis worldwide, with life-threatening complications if not managed correctly. Previous in vitro studies have utilized change in motility patterns of adult female worms to assess the efficacy of anthelmintics qualitatively. However, it is the third stage larvae (L3) that are infectious to humans. With differential staining using propidium iodide penetration as the indicator of death, we can distinguish between dead and live larvae. This assay has enabled us to quantify the in vitro efficacy of nine clinically established anthelmintics on A. cantonensis L3. All drugs were tested at a 1 mm concentration. Piperazine and niclosamide were ineffective in inducing larval death; however, albendazole sulfoxide, pyrantel pamoate, diethylcarbamazine, levamisole and praziquantel were effective as compared to unexposed controls (P < 0.05). Ivermectin and moxidectin did not induce significant levels of mortality, but they considerably reduced larval motility almost immediately. This study indicates the need for further in vivo studies to determine the optimal dose and time frame for post-infection treatment with anthelmintics that demonstrated efficacy.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Bettinger, JC, Carnell, L, Davies, AG and McIntire, SL (2004) The use of Caenorhabditis elegans In molecular neuropharmacology. International Review of Neurobiology 62, 195212.CrossRefGoogle ScholarPubMed
Bhaibulaya, M (1975) Comparative studies on the life history of Angiostrongylus Mackerrasae (Bhaibulaya, 1968) and Angiostrongylus cantonensis (Chen, 1935). International Journal of Parasitology 5, 720.CrossRefGoogle Scholar
Bisseru, B, Gill, SS and Lucas, JK (1972) Human infection with rat lung worm Angiostrongylus cantonensis (Chen, 1935) in West Malaysia. Medical Journal of Malaya 26, 164166.Google Scholar
Bowden, DK (1981) Eosinophilic meningitis in the New Hebrides: two outbreaks and two deaths. American Journal of Tropical Medicine and Hygiene 30, 11413.CrossRefGoogle ScholarPubMed
Campos, DMB, Barbosa, AP, Oliveira, JA, Barbosa, CAL, Lobo, TFC, Silva, LG, Thomaz, DV and de Castro, JP (2016) Evaluation of the therapeutic efficacy of levamisole hydrochloride on third-stage larvae of Lagochilascaris minor in experimentally infected mice. Revista do Instituto Medicina Tropical de São Paulo 58, 43.CrossRefGoogle ScholarPubMed
Chang, A, Osterloh, J and Thomas, J (2010) Levamisole: a dangerous new cocaine adulterant. Clinical Pharmacology and Therapeutics 88, 408411.CrossRefGoogle ScholarPubMed
Chen, WL, Zhong, JM, Chen, H, Wu, SY and Ding, L (2006) Eosinophilic meningitis: 31 cases report. Chinese Journal Misdiagnosis 6, 46684669.Google Scholar
Chen, W, Mook, RA Jr, Premont, RT and Wang, J (2018) Niclosamide: beyond an anthelminthic drug. Cellular Signaling 41, 8996.CrossRefGoogle Scholar
Children's Health Queensland Hospital and Health Services, Australia (2019) Prophylaxis against Angiostrongylus cantonensis infection. https://www.childrens.health.qld.gov.au/wp-content/uploads/PDF/ams/gdl-01219.pdf (Accessed 23 April 2020).Google Scholar
Chotmongkol, V, Wongjitrat, C, Sawadpanit, K and Sawanyawisuth, K (2004) Treatment of eosinophilic meningitis with a combination of albendazole and corticosteroid. Southeast Asian Journal of Tropical Medicine and Public Health 35, 172174.Google ScholarPubMed
Chotmongkol, V, Sawadpanitch, K, Sawanyawisuth, K, Louhawilai, S and Limpawattana, P (2006) Treatment of eosinophilic meningitis with a combination of prednisolone and mebendazole. American Journal of Tropical Medicine and Hygiene 74, 11221124.CrossRefGoogle ScholarPubMed
Cobb, R and Boeckh, A (2009) Moxidectin: a review of chemistry, pharmacokinetics and use in horses. Parasites and Vectors 2, 5.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Cuckler, AC, Egerton, JR and Alicata, JE (1964) Therapeutic effect of thiabendazole on Angiostrongylus cantonensis Infection in rats. Journal of Parasitology 51, 392396.CrossRefGoogle Scholar
Diao, Z, Wang, J, Qi, H, Li, X, Zheng, X and Yin, C (2011) Treatment of angiostrongyliasis using a combination of albendazole and dexamethasone: the results of a retrospective and comparative study. Annals of Tropical Medicine and Parasitology 105, 6569.CrossRefGoogle ScholarPubMed
Food and Drug Administration (2009) Prescribing information of albendazole. https://www.accessdata.fda.gov/drugsatfda_docs/label/2009/020666s005s006lbl.pdf (Accessed 23 April 2020).Google Scholar
Fru, MF and Puoti, A (2014) Acquired resistance to monepantel in C. elegans: what about parasitic nematodes? Worm 3, e959416.CrossRefGoogle Scholar
Gilleard, JS and Beech, RN (2007) Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 11331147. https://doi.org/10.1017/S0031182007000066.CrossRefGoogle ScholarPubMed
Graeff-Teixeira, C, da Silva, AC and Yoshimura, K (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22, 322348.CrossRefGoogle ScholarPubMed
Hammoud, RA, Nayes, SL, Murphy, JR, Heresi, GP, Butler, IJ and Pérez, N (2017) Angiostrongylus cantonensis meningitis and myelitis, Texas, USA. Emerging Infectious Disease 23, 10371038.CrossRefGoogle ScholarPubMed
Han, JH, Zhu, YH, Jie, WZ, Li, Y, Yan, Y, Ying, M and Xiong, J (2006) Eosinophilic meningitis: 28 cases report. Journal of Pathology and Disease Biology 1, 23.Google Scholar
Harrow, ID and Gration, KF (1985) Mode of action of the anthelmintics morantel, pyrantel and levamisole on muscle cell membrane of the nematode Ascaris suum. Pesticide Science 16, 662672.CrossRefGoogle Scholar
Hawai‘i Governor's Joint Task Force on Rat Lungworm Disease: Clinical Subcommittee (2018) Preliminary guidelines for diagnosis and treatment of human neuroangiostrongyliasis. https://health.hawaii.gov/docd/files/2018/08/RLWD_Preliminary_Clinical_Guidelines_FINAL_082918.pdf (Accessed 23 April 2020).Google Scholar
Hayashi, M (1987) Studies on chemotherapy of parasitic helminth (XXX); clinical and pathological changes in mice infected with Angiostrongylus cantonensis And treatment with mebendazole and betamethasone. Japanese Journal of Parasitology 36, 8087.Google Scholar
Hayashi, M, Terada, M, Ishii, A, Kino, H and Sano, M (1982) Studies on chemotherapy of parasitic helminths. (XVI). Anthelmintic effect of mebendazole on Angiostrongylus cantonensis in rats. Japanese Journal of Parasitology 31, 575580.Google Scholar
Hidelaratchi, M, Riffsy, M and Wijesekera, J (2010) A case of eosinophilic meningitis following monitor lizard meat consumption, exacerbated by anthelmintics. Ceylon Medical Journal 50, 8486.CrossRefGoogle Scholar
Hu, Y, Xiao, S and Aroian, RV (2009) The new anthelmintic tribendimidine is an L-type (levamisole and pyrantel) nicotinic acetylcholine receptor agonist. PLoS Neglected Tropical Disease 3, 499.CrossRefGoogle ScholarPubMed
Hwang, KP and Chen, ER (1988) Larvicidal effect of albendazole against Angiostrongylus cantonensis in mice. American Journal of Tropical Medicine and Hygiene 39, 191195.CrossRefGoogle ScholarPubMed
Iravani, J (1965) Wechselbeziehung von barbituraten und piperazin mit GABA an der membran des krebsmuskels. Naunyn–Schmiedeberg's Archives of Pharmacology 251, 265274.Google Scholar
Ishii, A (1994) Effect of anthelmintic levamisole on the first-stage of Angiostrongylus cantonensis in infected rats. Parasitology Research 80, 267270.Google Scholar
Ishii, AI, Terada, M and Sano, M (1985) Studies on chemotherapy of parasitic helminths. (XXII). Effects of ivermectin on Angiostrongylus cantonensis in rats. Japanese Journal of Parasitology 34, 411417.Google Scholar
Ismail, MM, Jayakody, RL, Weil, GJ, Nirmalan, N, Jayasinghe, KSA, Abeyewickrema, W, Rezvi Sheriff, MH, Rajaratnam, HN, Amarasekera, N, de Silva, DCL, Michalski, ML and Dissanaike, AS (1998) Efficacy of single dose combinations of albendazole, ivermectin and diethylcarbamazine for the treatment of bancroftian filariasis. Transactions of the Royal Society of Tropical Medicine Hygiene 92, 9497.CrossRefGoogle ScholarPubMed
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, Jacob, J, Sugihara, RT, Leinbach, IL, Klasner, IH, Kaluna, LM, Snook, KA, Howe, MH, Jacquier, SH, Lange, I, Atkinson, AL, Deane, AR, Niebuhr, CN and Siers, SR (2019) Validation of a death assay for Angiostrongylus cantonensis larvae (L3) using propidium iodide in a rat model (Rattus norvegicus). Parasitology 146, 18. doi:10.1017/S0031182019000908CrossRefGoogle 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.CrossRefGoogle Scholar
Jitpimolmard, S, Sawanyawisuth, K, Morakote, N, Morakote, N, Vejjajiva, A, Puntumetakul, M, Sanchaisuriya, K, Tassaneeyakul, W, Tassaneeyakul, W and Korwanich, N (2007) Albendazole therapy for eosinophilic meningitis caused by Angiostrongylus cantonensis. Parasitology Research 100, 12931296.CrossRefGoogle ScholarPubMed
Kliks, MM, Kroenke, K and Hardman, JM (1982) Eosinophilic radiculomyeloencephalitis: an angiostrongyliasis outbreak in American Samoa related to ingestion of Achatina fulica snails. American Journal of Tropical Medicine and Hygiene 31, 11141122.CrossRefGoogle ScholarPubMed
Lai, SC, Jiang, ST, Chen, KM, Hsu, JD, Shyu, LY and Lee, HH (2004) Efficacy of albendazole–GM6001 co-therapy against Angiostrongylus cantonensis induced meningitis in BALB/c mice. Acta Tropica 93, 267273.CrossRefGoogle Scholar
Lakwo, TT, Ishih, A, Terada, M and Sano, M (1998) Effects of albendazole against larval and adult Angiostrongylus cantonensis in rat. Parasitology International 47, 281288.CrossRefGoogle Scholar
Lan, KP, Wang, CJ, Lai, SC and Chen, KM (2004) The efficacy of therapy with albendazole in mice with parasitic meningitis caused by Angiostrongylus cantonensis. Parasitology Research 93, 311317.CrossRefGoogle ScholarPubMed
Leone, S, De Marco, M, Ghirga, P, Nicastri, E, Esposito, M and Narciso, P (2007) Eosinophilic meningitis in a returned traveler from Santo Domingo: case report and review. Journal of Travel Medicine 14, 407410.CrossRefGoogle Scholar
Li, H, Xu, F, Gu, JB and Chen, XG (2008) Case report: a severe eosinophilic meningoencephalitis caused by infection of Angiostrongylus cantonensis. American Journal of Tropical Medicine and Hygiene 79, 568570.CrossRefGoogle ScholarPubMed
Liu, X, Chen, Y, Chen, X, Su, J and Huang, C (2019) Enhanced efficacy of baicalin-loaded TPGS polymeric micelles against periodontitis. Materials Science and Engineering: C 101, 387395.CrossRefGoogle ScholarPubMed
Lovell, RA (1990) Ivermectin and piperazine toxicosis in dogs and cats. Veterinary Clinics of North America. Small Animal Practice 20, 453468.CrossRefGoogle Scholar
Lv, S, Zhang, Y, Liu, H, Zhang, C, Steinmann, P, Zhou, X and Utzinger, U (2009) Angiostrongylus cantonensis: morphological and behavioral investigation within the freshwater snail Pomacea canaliculate. Parasitology Research 104, 13511359.CrossRefGoogle Scholar
Ma, M, Zhang, M and Qiu, Z (2018) Eosinophilic meningitis caused by Angiostrongylus cantonensis in an infant. Medicine 97, e10975.CrossRefGoogle ScholarPubMed
Mackerras, MJ and Sandars, DF (1955) The life-history of the rat lungworm, Angiostrongylus cantonensis (Chen) (Nematoda: Metastrongylidae). Australian Journal of Zoology 3, 121.CrossRefGoogle Scholar
Martin, RJ and Geary, TG (2016) Pharmacology of pyrantel. In Marchiondo, AA (ed.), Pyrantel Parasiticide Therapy in Humans and Domestic Animals. Massachusetts, USA: Academic Press, pp. 2145.CrossRefGoogle Scholar
Martin, RJ, Valkanov, MA, Dale, VM, Robertson, AP and Murray, I (1996) Electro-physiology of Ascaris muscle and anti-nematodal drug action. Parasitology 113, 137156.CrossRefGoogle Scholar
McAuliffe, L, Ensign, SF, Larson, D, Bavaro, M, Yetto, J, Cathey, M, Mukaigawara, M, Narita, M, Ohkusu, K, Quast, T and Volk, C (2019) Severe CNS angiostrongyliasis in a young marine: a case report and literature review. Lancet Infectious Diseases 19, e132e142.CrossRefGoogle Scholar
Mentz, MB and Graeff-Teixeira, C (2003) Drug trials for treatment of human angiostrongyliasis (review). Revista do Instituto Medicina Tropical de São Paulo 45, 179184.CrossRefGoogle Scholar
Morganti-Kossmann, MC, Rancan, M, Stahel, PF and Kossmann, T (2002) Inflammatory response in acute traumatic brain injury: a double-edged sword. Current Opinion in Critical Care 8, 101105.CrossRefGoogle ScholarPubMed
Murphy, GS and Johnson, S (2013) Clinical aspects of eosinophilic meningitis and meningoencephalitis caused by Angiostrongylus cantonensis, the rat lungworm. Hawaii Journal of Medicine and Public Health 72, 3540.Google ScholarPubMed
Olliaro, PL, Kuesel, AC, Halleux, CM, Sullivan, M and Reeder, JC (2018) Creative use of the priority review voucher by public and not-for-profit actors delivers the first new FDA-approved treatment for river blindness in 20 years. PLoS Neglected Tropical Diseases 12, e0006837.CrossRefGoogle ScholarPubMed
Page, SW (2008) Antiparasitic drugs. In Maddison, JE, Page, SW and Church, DB (eds), Small Animal Clinical Pharmacology, 2nd Edn. Pennsylvania, USA: Saunders Ltd, pp. 198260.CrossRefGoogle Scholar
Perry, NR and Moens, M (2011) Survival of parasitic nematodes outside the host. In Perry, NR and Moens, M (Eds), Molecular and Physiological Basis of Nematode Survival. Wallingford, UK: CABI Publishing, pp. 127.CrossRefGoogle Scholar
Pickering, LK, Baker, CJ, Long, SS and McMillan, JA (2006) American Academy of pediatrics. Pinworm infection. In Pickering, LK, Baker, CJ, Long, SS and McMillan, JA (eds), Red Book: Report of the Committee on Infectious Diseases, 27th Edn. Illinois, USA: American academy of pediatrics, pp. 520522.Google Scholar
Pien, FD and Pien, BC (1999) Angiostrongylus cantonensis eosinophilic meningitis. International Journal of Infectious Diseases 3, 161163.CrossRefGoogle ScholarPubMed
Prichard, R, Menez, C and Lespine, A (2012) Moxidectin and the avermectins: consanguinity but not identity. International Journal for Parasitology. Drugs and Drug Resistance 2, 134153.CrossRefGoogle Scholar
Prociv, P and Turner, M (2018) Neuroangiostrongyliasis: the “subarachnoid phase” and its implications for anthelmintic therapy. American Journal of Tropical Medicine and Hygiene 98, 353359.CrossRefGoogle Scholar
Qvarnstrom, Y, Xayavong, M, da Silva, AC, Park, SY, Whelen, AC, Calimlim, PS, Sciulli, RH, Honda, SAA, Higa, K, Kitsutani, P, Chea, N, Heng, S, Johnson, S, Graeff-Teixeira, C, Fox, LM and da Silva, AJ (2016) Real-time polymerase chain reaction detection of Angiostrongylus cantonensis DNA in cerebrospinal fluid from patients with eosinophilic meningitis. American Journal of Tropical Medicine and Hygiene 9, 176181.CrossRefGoogle Scholar
Ramirez, T, Benitez-Bribiesca, L, Ostrosky-Wegman, P and Herrera, LA (2001) In vitro effects of albendazole and its metabolites on the cell proliferation kinetics and micronuclei frequency of stimulated human lymphocytes. Archives of Medical Research 32, 119122.CrossRefGoogle ScholarPubMed
Reinemeyer, CR (2016) Formulations and clinical uses of pyrimidine compounds in domestic animals. In Marchiondo, AA (ed.), Pyrantel Parasiticide Therapy in Humans and Domestic Animals. Massachusetts, USA: Academic Press, pp. 67107.CrossRefGoogle Scholar
Roland, N, Fritz, S and Helmut, E (2010) Penetration of drugs through the blood-cerebrospinal fluid/blood-brain barrier for treatment of central nervous system infections. Clinical Microbiology Reviews 23, 858883.Google Scholar
Saari, S, Näreaho, A and Nikander, S (2019) Therapy and control. In Saari, S, Näreaho, A and Nikander, S (eds), Canine Parasites and Parasitic Disease. Massachusetts, USA: Academic Press, pp. 247254.CrossRefGoogle Scholar
Shalaby, HA (2013) Anthelmintics resistance; How to overcome it? Iranian Journal of Parasitology 8, 1832.Google Scholar
Sharma, S and Anand, N (1997) Tetrahydropyrimidines. In Sharma, S and Anand, N (Eds), Approaches to Design and Synthesis of Antiparasitic Drugs, vol. 25. Amsterdam: Pharmacochemistry Library, pp. 171180.CrossRefGoogle Scholar
Sheehan, DJ, Sheehan, SM and Marchiondo, AA (2016) Discovery and chemistry of pyrantel, morantel and oxantel. In Marchiondo, AA (ed.), Pyrantel Parasiticide Therapy in Humans and Domestic Animals. Massachusetts, USA: Academic Press, pp. 119.Google Scholar
Singh, M, McKenzie, K and Ma, X (2017) Effect of dimethyl sulfoxide on in vitro Proliferation of skin fibroblast cells. Journal of Biotechnology Research 8, 7882.Google Scholar
Stockdale, HD, Slapcinsky, JD, Roff, S, Mendieta, CJ, Diaz, GZ and Stern, J (2017) Geographic distribution of Angiostrongylus cantonensis in wild rats (Rattus Rattus) and terrestrial snails in Florida, USA. PLoS One 12, e0177910.CrossRefGoogle 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. Hawaii Journal of Medicine and Public Health 72, 1114.Google ScholarPubMed
Terada, M and Sano, M (1986) Effects of diethylcarbamazine on the motility of Angiostrongylus cantonensis and Dirofilaria immitis. Zeitschrift für Parasitenkunde 72, 375385.CrossRefGoogle ScholarPubMed
Terada, M, Shii, AI, Kino, H and Sano, M (1982) Studies on chemotherapy of parasitic helminths (VII). Effects of various cholinergic agents on the motility of Angiostrongylus cantonensis. Japanese Journal of Pharmacology 32, 633642.CrossRefGoogle ScholarPubMed
Terada, M, Shii, AI, Kino, H and Sano, M (1983) Studies on chemotherapy of parasitic helminth (XVIII). Mechanism of spastically paralyzing action of pyrantel in Angiostrongylus cantonensis. Experientia 39, 13831385.CrossRefGoogle ScholarPubMed
Terada, M, Ishii, AI, Kino, H and Sano, M (1984) Angiostrongylus cantonensis: paralysis due to avermectin B1a and ivermectin. Experimental Parasitology 57, 149157.CrossRefGoogle ScholarPubMed
Terada, M, Rodrigues, BO, Dharejo, AM, Shii, AI and Sano, M (1986) Studies on chemotherapy of parasitic helminths (XXVI). Comparative in vitro effects if various anthelmintics on the motility of Angiostrongylus costaricensis and A. cantonensis. Japanese Journal of Parasitology 35, 365367.Google Scholar
Thomas, CM and Timson, D (2020) The mechanism of action of praziquantel: can new drugs exploit similar mechanisms? Current Medicinal Chemistry 27, 676696.CrossRefGoogle ScholarPubMed
Tu, WC and Lai, SC (2006) Angiostrongylus cantonensis: efficacy of albendazole-dexamethasone co-therapy against infection-induced plasminogen activators and eosinophilic meningitis. Experimental Parasitology 113, 815.CrossRefGoogle ScholarPubMed
Vermund, SH, MacLeod, S and Goldstein, RG (1986) Taeniasis unresponsive to a single dose of niclosamide: case report of persistent infection with Taenia saginata and a review of therapy. Reviews of Infectious Diseases 8, 423426.CrossRefGoogle Scholar
Waller, DG and Sampson, AP (2018) Chemotherapy of infections. In Waller, DG and Sampson, AP (Eds), Medical Pharmacology and Therapeutics, 5th Edn. Amsterdam: Elsevier, pp. 581629.CrossRefGoogle Scholar
Wang, LC, Chao, D and Chen, ER (1991) Experimental infection routes of Angiostrongylus cantonensis in mice. Journal of Helminthology 65, 296300.CrossRefGoogle ScholarPubMed
Wang, LC, Jung, SM, Chen, CC, Wong, HF, Wan, DP and Wan, YL (2006) Pathological changes in the brain of rabbits experimentally infected with Angiostrongylus cantonensis after albendazole treatment: histopathological and magnetic resonance imaging studies. Journal of Antimicrobial Chemotherapy 57, 294300.CrossRefGoogle ScholarPubMed
Wang, PQ, Lai, DH, Zhu, XQ, Chen, XG and Lun, ZR (2008) Human angiostrongyliasis. Lancet Infectious Diseases 8, 621630.CrossRefGoogle ScholarPubMed
Wang, J, Qi, H, Diao, Z, Zheng, X, Li, X, Ma, S, Ji, A and Yin, C (2010) An outbreak of Angiostrongylus cantonensis in Beijing. Journal of Parasitology 96, 377381.CrossRefGoogle ScholarPubMed
World Health Organization (2019) Essential medicines list 21st edition. https://www.who.int/medicines/publications/essentialmedicines/en/ (Accessed 23 April 2020).Google Scholar