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The effects of temperature and salinity on the longevity of Opisthorchis viverrini cercariae: a climate change concern

Published online by Cambridge University Press:  23 June 2020

S. Prasopdee Open the ORCID record for S. Prasopdee [Opens in a new window] ,
J. Kulsantiwong ,
T. Sathavornmanee Open the ORCID record for T. Sathavornmanee [Opens in a new window]  and
V. Thitapakorn
S. Prasopdee*
Affiliation:
Research Group in Development of Diagnosis and Targeted Therapeutics for Opisthorchis viverrini and Cholangiocarcinoma, Chulabhorn International College of Medicine, Thammasat University, Klong Luang, Pathum Thani12120, Thailand
J. Kulsantiwong
Affiliation:
Department of Biology, Faculty of Science, Udon Thani Rajabhat University, Udon Thani41000, Thailand
T. Sathavornmanee
Affiliation:
Research Group in Development of Diagnosis and Targeted Therapeutics for Opisthorchis viverrini and Cholangiocarcinoma, Chulabhorn International College of Medicine, Thammasat University, Klong Luang, Pathum Thani12120, Thailand
V. Thitapakorn
Affiliation:
Research Group in Development of Diagnosis and Targeted Therapeutics for Opisthorchis viverrini and Cholangiocarcinoma, Chulabhorn International College of Medicine, Thammasat University, Klong Luang, Pathum Thani12120, Thailand
*
Author for correspondence: S. Prasopdee, E-mail: [email protected]
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Abstract

Research on the effects of environmental factors influenced by climate change on parasite transmissibility is an area garnering recent attention worldwide. However, there is still a lack of studies on the life cycle of Opisthorchis viverrini, a carcinogenic trematode found in countries of the Lower Mekong subregion of Lao PDR, Cambodia, Myanmar, Vietnam and Thailand. To evaluate the influences of environmental factors water temperature and salinity on the transmissibility of the liver fluke O. viverrini through cercarial stage, longevity of O. viverrini cercaria was examined at different experimental temperatures (22°C, 30°C and 38°C) and salinities (2.5 parts per thousand (PPT), 3.75 PPT and 5 PPT). The results reveal that different temperatures have statistically significant effects on cercarial longevity. The cercariae exhibited a thermostability zone ranging between 22°C and 30°C. Cercarial longevity was significantly shortened when water temperatures reached 38°C. Salinity also plays a key role in cercarial longevity, with cercarial survival significantly shorter at a salinity of 3.75 PPT than at 2.5 PPT and 5 PPT. A combined analysis of salinity and temperature revealed unique trends in cercarial longevity. At all experimental salinities, cercarial longevity was lowest when incubated in 38°C, but statistically significant from cercarial longevity at temperatures of 22°C and 30°C, and salinities of 2.5 PPT and 5 PPT. The results suggest that higher temperatures negatively impact parasite longevity. This reflects that O. viverrini transmission patterns may be impacted by changes in water temperature and salinity resulting from climate change.

Keywords

Opisthorchis viverrinitemperaturesalinityclimate changecercarial transmissioncholangiocarcinoma
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e165
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Anderson, RM and Whitfield, PJ (1974) Proceedings: a model for the survival rate of non-feeding larval parasites. Parasitology 69, 7.Google Scholar
Andrews, RH, Sithithaworn, P and Petney, TN (2008) Opisthorchis viverrini: an underestimated parasite in world health. Trends in Parasitology 24, 497–501.CrossRefGoogle ScholarPubMed
Aung, WPP, Htoon, TT, Tin, HH, et al. (2017) First report and molecular identification of Opisthorchis viverrini infection in human communities from Lower Myanmar. PLOS ONE 12, e0177130.CrossRefGoogle ScholarPubMed
Aunpromma, S, Tangkawattana, P, Papirom, P, Kanjampa, P, Tesana, S, Sripa, B and Tangkawattana, S (2012) High prevalence of Opisthorchis viverrini infection in reservoir hosts in four districts of Khon Kaen Province, an opisthorchiasis endemic area of Thailand. Parasitology International 61, 60–64.CrossRefGoogle Scholar
Barber, I, Berkhout, BW and Ismail, Z (2016) Thermal change and the dynamics of multi-host parasite life cycles in aquatic ecosystems. Integrative and Comparative Biology 56, 561–572.CrossRefGoogle ScholarPubMed
Bouvard, V, Baan, R, Straif, K, et al. (2009) A review of human carcinogens–Part B: biological agents. Lancet Oncology 10, 321–322.CrossRefGoogle ScholarPubMed
Brockelman, WY, Upatham, ES, Viyanant, V, Ardsungnoen, S and Chantanawat, R (1986) Field studies on the transmission of the human liver fluke, Opisthorchis viverrini, in northeast Thailand: population changes of the snail intermediate host. International Journal for Parasitology 16, 545–552.CrossRefGoogle ScholarPubMed
Enes, JE, Wages, AJ, Malone, JB and Tesana, S (2010) Prevalence of Opisthorchis viverrini infection in the canine and feline hosts in three villages, Khon Kaen Province, northeastern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 41, 36–42.Google Scholar
Frandsen, F and Christensen, NO (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Tropica 41, 181–202.Google ScholarPubMed
Ginetsinskaya, T (1960) The relationship between the distribution of glycogen in the bodies of different cercariae and their biological peculiarities. Doklady Biological Sciences 135, 949–951.Google Scholar
Ginetsinskaya, T (1988) Trematodes, their life cycles, biology and evolution. 559 pp. New Delhi, Amerind Publishing Company.Google Scholar
Hansen, J, Sato, M, Ruedy, R, Lo, K, Lea, WW and Medina-Elizade, M (2006) Global temperature change. Proceedings of the National Academy of Sciences of the United States of America 103, 14288–14293.CrossRefGoogle ScholarPubMed
Harinasuta, C and Harinasuta, T (1984) Opisthorchis viverrini: life cycle, intermediate hosts, transmission to man and geographical distribution in Thailand. Arzneimittelforschung 34, 1164–1167.Google Scholar
Haswell-Elkins, MR, Mairiang, E, Mairiang, P, Chaiyakum, J, Chamadol, N, Loapaiboon, V, Sithithaworn, P and Elkins, DB (1994) Cross-sectional study of Opisthorchis viverrini infection and cholangiocarcinoma in communities within a high-risk area in northeast Thailand. International Journal of Cancer 59, 505–509.CrossRefGoogle ScholarPubMed
IARC (2002) Cancer incidence in five continents. Vol. 8. Lyon, France, IARC Scientific Publication, 1–781.Google Scholar
Jongsuksuntigul, P and Imsomboon, T (2003) Opisthorchiasis control in Thailand. Acta Tropica 88, 229–232.CrossRefGoogle ScholarPubMed
Keiser, J and Utzinger, J (2009) Food-borne trematodiases. Clinical Microbiology Reviews 22, 466–483.CrossRefGoogle ScholarPubMed
Kiatsopit, N, Sithithaworn, P, Saijuntha, W, Boonmars, T, Tesana, S, Sithithaworn, J, Petney, TN and Andrews, RH (2012) Exceptionally high prevalence of infection of Bithynia siamensis goniomphalos with Opisthorchis viverrini cercariae in different wetlands in Thailand and Lao PDR. American Journal of Tropical Medicine and Hygiene 86, 464–469.CrossRefGoogle ScholarPubMed
Kiatsopit, N, Sithithaworn, P, Kopolrat, K, Andrews, RH and Petney, TN (2014) Seasonal cercarial emergence patterns of Opisthorchis viverrini infecting Bithynia siamensis goniomphalos from Vientiane Province, Lao PDR. Parasites & Vectors 7, 551.CrossRefGoogle ScholarPubMed
Kim, CS, Echaubard, P, Suwannatrai, A, Kaewkes, S, Wilcox, BA and Sripa, B (2016) Seasonal and spatial environmental influence on Opisthorchis viverrini intermediate hosts, abundance, and distribution: insights on transmission dynamics and sustainable control. PLOS Neglected Tropical Diseases 10, e0005121.CrossRefGoogle ScholarPubMed
Koprivnikar, J, Lim, D, Fu, C and Brack, SH (2010) Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitology Research 106, 1167–1177.CrossRefGoogle ScholarPubMed
Lowenberger, CA and Rau, ME (1994) Plagiorchis elegans: emergence, longevity and infectivity of cercariae, and host behavioural modifications during cercarial emergence. Parasitology 109(Pt. 1), 65–72.CrossRefGoogle ScholarPubMed
McCarthy, AM (1999) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118(Pt. 4), 383–388.CrossRefGoogle Scholar
Morley, NJ (2011) Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 1442–1452.CrossRefGoogle Scholar
Mouritsen, KN (2002) The Hydrobia ulvae-Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76, 341–347.CrossRefGoogle ScholarPubMed
Poulin, R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.CrossRefGoogle ScholarPubMed
Prasopdee, S (2013) Differential protein expression of Bithynia siamensis goniomphalos snail upon infection with liver fluke, Opisthorchis viverrini, a thesis for the degree of doctor of philosophy. p. 174. Khon Kaen University, Khon Kaen.Google Scholar
Prasopdee, S, Kulsantiwong, J, Piratae, S, et al. (2015) Temperature dependence of Opisthorchis viverrini infection in first intermediate host snail, Bithynia siamensis goniomphalos. Acta Tropica 141, 112–117.CrossRefGoogle ScholarPubMed
Purnell, RE (1966) Host-parasite relationships in schistosomiasis. 3. The effect of temperature on the survival of Schistosoma mansoni miracidia and on the survival and infectivity of Schistosoma mansoni cercariae. Annals of Tropical Medicine and Parasitology 60, 182–186.CrossRefGoogle ScholarPubMed
Rees, G (1948) A study of the effect of light, temperature and salinity on the emergence of Cercaria purpurae Lebour from Nucella lapillus (L). Parasitology 38, 228–242.CrossRefGoogle Scholar
Sithithaworn, P and Haswell-Elkins, M (2003) Epidemiology of Opisthorchis viverrini. Acta Tropica 88, 187–194.CrossRefGoogle ScholarPubMed
Sithithaworn, P, Pipitgool, V, Srisawangwong, T, Elkins, DB and Haswell-Elkins, MR (1997) Seasonal variation of Opisthorchis viverrini infection in cyprinoid fish in north-east Thailand: implications for parasite control and food safety. Bulletin of the World Health Organization 75, 125–131.Google ScholarPubMed
Sithithaworn, P, Andrews, RH, Nguyen, VD, et al. (2012) The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitology International 61, 10–16.CrossRefGoogle ScholarPubMed
Sri-Aroon, P, Butraporn, P, Limsomboon, J, Kerdpuech, Y, Kaewpoolsri, M and Kiatsiri, S (2005) Freshwater mollusks of medical importance in Kalasin Province, northeast Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 36, 653–657.Google ScholarPubMed
Stocker, TF, Qin, D and Plattner, GK (2013) Climate change 2013: the physical science basis. Working Group I contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA.Google Scholar
Studer, A and Poulin, R (2013) Cercarial survival in an intertidal trematode: a multifactorial experiment with temperature, salinity and ultraviolet radiation. Parasitology Research 112, 243–249.CrossRefGoogle Scholar
Suwannatrai, A, Suwannatrai, K, Haruay, S, et al. (2011) Effect of soil surface salt on the density and distribution of the snail Bithynia siamensis goniomphalos in northeast Thailand. Geospatial Health 5, 183–190.CrossRefGoogle ScholarPubMed
Thieltges, DW and Rick, J (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 63–68.Google Scholar
Traub, RJ, Macaranas, J, Mungthin, M, Leelayoova, S, Cribb, T, Murrell, KD and Thompson, RC (2009) A new PCR-based approach indicates the range of Clonorchis sinensis now extends to Central Thailand. PLoS Neglected Tropical Diseases 3, e367.CrossRefGoogle ScholarPubMed
Vichasri, S, Viyanant, V and Upatham, ES (1982) Opisthorchis viverrini: intensity and rates of infection in cyprinoid fish from an endemic focus in Northeast Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 13, 138–141.Google ScholarPubMed
Vonghachack, Y, Odermatt, P, Taisayyavong, K, Phounsavath, S, Akkhavong, K and Sayasone, S (2017) Transmission of Opisthorchis viverrini, Schistosoma mekongi and soil-transmitted helminthes on the Mekong Islands, Southern Lao PDR. Infectious Diseases of Poverty 6, 131.CrossRefGoogle ScholarPubMed
WHO (1995) Control of foodborne trematode infections. Report of a WHO Study Group. World Health Organization technical report series 849, 1–157.Google Scholar
Wongratanacheewin, S, Pumidonming, W, Sermswan, RW and Maleewong, W (2001) Development of a PCR-based method for the detection of Opisthorchis viverrini in experimentally infected hamsters. Parasitology 122, 175–180.CrossRefGoogle ScholarPubMed
Wykoff, DE, Harinasuta, C, Juttijudata, P and Winn, MM (1965) Opisthorchis viverrini in Thailand–the life cycle and comparison with O. Felineus. Journal of Parasitology 51, 207–214.CrossRefGoogle Scholar
Zander, CD (1998) Ecology of host parasite relationships in the Baltic Sea. Naturwissenschaften 85, 426–436.CrossRefGoogle ScholarPubMed