Efficacy of x-ray phytosanitary irradiation on the infectivity and reproduction of Angiostrongylus cantonensis in experimentally infected rats

Authors: JARVI, S - University Of Hawaii; KALUNA, L - University Of Hawaii; HESS, S - Animal And Plant Health Inspection Service (APHIS); Hamilton, Lindsey; ANTAKY, C - Animal And Plant Health Inspection Service (APHIS); SUGIHARA, R - Animal And Plant Health Inspection Service (APHIS); LEINBACH, I - University Of Hawaii; TAGAMI, Y - University Of Hawaii; STEEL, A - University Of Hawaii; HOWE, K - University Of Hawaii; JACQUIER, S - University Of Hawaii; COOKMAN, F - University Of Hawaii; DIAZ, JOCELYN - University Of Hawaii; JACOB, J - University Of Hawaii; Follett, Peter

Submitted to: American Journal of Tropical Medicine and Hygiene
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/29/2023
Publication Date: 2/20/2024
Citation: Jarvi, S., Kaluna, L.M., Hess, S.C., Hamilton, L.J., Antaky, C., Sugihara, R.T., Leinbach, I.L., Tagami, Y., Steel, A., Howe, K., Jacquier, S., Cookman, F., Diaz, J., Jacob, J., Follett, P.A. 2024. Efficacy of x-ray phytosanitary irradiation on the infectivity and reproduction of Angiostrongylus cantonensis in experimentally infected rats. American Journal of Tropical Medicine and Hygiene. 110(4):691-699. https://doi.org/10.4269/ajtmh.23-0570.
DOI: https://doi.org/10.4269/ajtmh.23-0570

Interpretive Summary: Angiostrongylus cantonensis is a globally-distributed nematode and the leading cause of eosinophilic meningitis in humans (aka, rat lungworm disease [RLW]). This nematode is found in several snail and slug hosts which can be found on agriculture produce exported from Hawaii, including sweet potatoes and several tropical fruits. Hawaii is a global hot spot for RLW, and its agricultural exports may be contributing to the spread of A. cantonensis. Sweet potatoes and various tropical fruits are exported to the continental United States using phytosanitary irradation at 150 Gy or 400 Gy to control quarantine pests. We tested whether these irradiation treatments would also stop reproduction in the nematode causing RLW by feeding irradiated nematodes to rats. X-ray irradiation did not cause direct mortality of nematode larvae, however, it did affect the infectivity and reproduction of the nematode within its definitive host, the rat. Thus, phytosanitary irradiation at doses =150 Gy appears as an effective means of preventing the establishment and spread of A. cantonensis.

Technical Abstract: Angiostrongylus cantonensis is a globally-distributed nematode and the leading cause of eosinophilic meningitis in humans. As a global hotspot for this disease, Hawaii’s agricultural exports may be contributing to the spread of A. cantonensis. Phytosanitary irradiation doses of 150 or 400 Gy provide quarantine security against pests such as tephritid fruit flies and other insects internationally as well as within the US. We evaluated the in vitro and in vivo effects of phytosanitary irradiation on the infectious, third-stage A. cantonensis larvae. In vitro experiments directly exposed larvae to irradiation doses ranging from 200 to 1000 Gy. Results showed low mortality and no dose-response across all treatments 27 days post-irradiation. In vivo studies isolated larvae from wild-caught Parmarion martensi after the semi-slugs were exposed to x-ray irradiation at doses of 0 Gy, 150 Gy and 400 Gy, and infected them into laboratory rats. Fourteen rats were assigned to each treatment and infected with 50 larvae from their assigned irradiation dose. Results at three- and six-weeks post-infection demonstrated a significant negative dose-response in regard to the number of larvae that migrated to the brain and the number of adults found in the pulmonary artery. Within each treatment no significant differences were found between the number of A. cantonensis observed in the brain and pulmonary artery, indicating that most irradiated larvae which successfully migrated to the brain were able to grow into adults. No irradiated larvae that grew into adults were able to produce eggs. These findings indicate that x-ray irradiation does not result in the direct mortality of A. cantonensis larvae, however, it does affect the infectivity and reproduction of A. cantonensis within its definitive host, the rat. Thus, phytosanitary irradiation at doses =150 Gy appears as an effective means of preventing the establishment of viable populations of A. cantonensis.