Epidemiology of Strongyloides stercoralis and Opisthorchis viverrini infections in northern and northeastern Thailand: Insights from urine-ELISA surveys.

Publisher: Springer International Country of Publication: Germany NLM ID: 8703571 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-1955 (Electronic) Linking ISSN: 09320113 NLM ISO Abbreviation: Parasitol Res Subsets: MEDLINE

Original Publication: Berlin : Springer International, c1987-

Strongyloides stercoralis*/isolation & purification ; Opisthorchis* ; Strongyloidiasis*/epidemiology ; Strongyloidiasis*/urine ; Strongyloidiasis*/parasitology ; Opisthorchiasis*/epidemiology ; Opisthorchiasis*/parasitology ; Opisthorchiasis*/urine ; Enzyme-Linked Immunosorbent Assay*; Humans ; Thailand/epidemiology ; Animals ; Male ; Female ; Middle Aged ; Adult ; Cross-Sectional Studies ; Prevalence ; Adolescent ; Young Adult ; Aged ; Child ; Risk Factors ; Child, Preschool ; Aged, 80 and over ; Infant

Strongyloides stercoralis and Opisthorchis viverrini are helminth parasites responsible for significantly neglected tropical diseases. This study aimed to evaluate the prevalence of these parasites and the risk factors for S. stercoralis and O. viverrini infections in northern and northeastern Thailand where relevant epidemiological data are scarce and outdated. A cross-sectional study was conducted in 2016 in six sub-districts across five provinces. Urine samples were analyzed to detect S. stercoralis and O. viverrini infection using urine enzyme-linked immunosorbent assays (urine-ELISA). Demographic data of participants were collected using a questionnaire. Environmental data, including land-surface temperature (LST), normalized difference vegetation index (NDVI), normalized difference water index (NDWI), and soil pH, were obtained from remote-sensing sources. Multiple logistic regression analysis identified risk factors associated with infection. Complete data were obtained for 2613 individuals. The overall prevalence was 39.15% (95% CI: 37.27-41.02) for S. stercoralis and 37.46% (95% CI: 35.61-39.32) for O. viverrini. Male sex was significantly associated with S. stercoralis (AOR, 1.53; 95% CI, 1.29-1.80, p < 0.001) and O. viverrini infections (AOR, 1.69; 95% CI, 1.43-2.00, p < 0.001). The prevalence of S. stercoralis infection increased with age. Spatially, the odds of S. stercoralis infection decreased with higher LST and soil pH, while O. viverrini infection was associated with higher soil pH and proximity to water bodies. Strongyloides stercoralis and O. viverrini are highly prevalent in these regions, highlighting the need for surveillance.
Competing Interests: Declarations. The study protocol was approved by the Khon Kaen University Ethics Committee for Human Research (HE631478) and adhered to the principles of the Declaration of Helsinki on Human Rights (1975). The CASCAP project received approval from Khon Kaen University Ethics Committee for Human Research under the reference number HE601370. All patients gave written informed consent for the CASCAP study. Consent for publication: Not applicable. Competing interests: The authors declare no competing interests.
(© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Anamnart W, Intapan PM, Maleewong W (2013) Modified formalin-ether concentration technique for diagnosis of human strongyloidiasis. Korean J Parasitol 51(6):743–745. https://doi.org/10.3347/kjp.2013.51.6.743. (PMID: 10.3347/kjp.2013.51.6.743245162833916467)
Arjyal A, Parajuli A, Kharel C, Del Barrio MO, Baral SC (2023) Understanding gender and its intersection with social stratifiers on prevention and care seeking behavior of lymphatic filariasis in Nepal. Infect Dis Poverty 12(1):77. https://doi.org/10.1186/s40249-023-01126-8. (PMID: 10.1186/s40249-023-01126-83760833210463999)
Blum AJ, Hotez PJ (2018) Global “worming”: climate change and its projected general impact on human helminth infections. PLoS Negl Trop Dis 12(7):e0006370. https://doi.org/10.1371/journal.pntd.0006370. (PMID: 10.1371/journal.pntd.0006370300248716053132)
Bryant AS, Hallem EA (2018) Temperature-dependent behaviors of parasitic helminths. Neurosci Lett 687:290–303. https://doi.org/10.1016/j.neulet.2018.10.023. (PMID: 10.1016/j.neulet.2018.10.023303361966240462)
Buonfrate D et al (2020) The global prevalence of strongyloides stercoralis infection. Pathogens 9(6). https://doi.org/10.3390/pathogens9060468.
Buonfrate D, Bradbury RS, Watts MR, Bisoffi Z (2023) Human strongyloidiasis: complexities and pathways forward. Clin Microbiol Rev 36(4):e0003323. https://doi.org/10.1128/cmr.00033-23. (PMID: 10.1128/cmr.00033-2337937980)
Chaicumpa W et al (1992) Detection of Opisthorchis viverrini antigens in stools using specific monoclonal antibody. Int J Parasitol 22(4):527–531. https://doi.org/10.1016/0020-7519(92)90155-e. (PMID: 10.1016/0020-7519(92)90155-e1644529)
Charoensuk L, Subrungruang I, Mungthin M, Pinlaor S, Suwannahitatorn P (2019) Comparison of stool examination techniques to detect Opisthorchis viverrini in low intensity infection. Acta Trop 191:13–16. https://doi.org/10.1016/j.actatropica.2018.12.018. (PMID: 10.1016/j.actatropica.2018.12.01830550733)
Czeresnia JM, Weiss LM (2022) Strongyloides stercoralis. Lung 200(2):141–148. https://doi.org/10.1007/s00408-022-00528-z. (PMID: 10.1007/s00408-022-00528-z353969578994069)
Eamudomkarn C et al (2018) Diagnostic performance of urinary IgG antibody detection: a novel approach for population screening of strongyloidiasis. PLoS One 13(7):e0192598. https://doi.org/10.1371/journal.pone.0192598. (PMID: 10.1371/journal.pone.0192598299859136037348)
Eamudomkarn C, Sithithaworn P, Sithithaworn J, Kaewkes S, Sripa B, Itoh M (2015) Comparative evaluation of Strongyloides ratti and S. stercoralis larval antigen for diagnosis of strongyloidiasis in an endemic area of opisthorchiasis. Parasitol Res 114(7):2543–51. https://doi.org/10.1007/s00436-015-4458-3.
Fleitas PE et al (2022) Mapping the global distribution of Strongyloides stercoralis and hookworms by ecological niche modeling. Parasit Vectors 15(1):197. https://doi.org/10.1186/s13071-022-05284-w. (PMID: 10.1186/s13071-022-05284-w356767409178904)
Forrer A et al (2017) Strongyloides stercoralis is associated with significant morbidity in rural Cambodia, including stunting in children. PLoS Negl Trop Dis 11(10):e0005685. https://doi.org/10.1371/journal.pntd.0005685. (PMID: 10.1371/journal.pntd.0005685290591955695629)
Forrer A et al (2019) Strongyloides stercoralis: Spatial distribution of a highly prevalent and ubiquitous soil-transmitted helminth in Cambodia. PLoS Negl Trop Dis 13(6):e0006943. https://doi.org/10.1371/journal.pntd.0006943. (PMID: 10.1371/journal.pntd.0006943312200756586258)
Forrer A et al (2012) Spatial distribution of, and risk factors for, Opisthorchis viverrini infection in southern Lao PDR. PLoS Negl Trop Dis 6(2):e1481. https://doi.org/10.1371/journal.pntd.0001481. (PMID: 10.1371/journal.pntd.0001481223481573279336)
Gordon CA et al (2024) Strongyloidiasis. Nat Rev Dis Primers 10(1):6. https://doi.org/10.1038/s41572-023-00490-x. (PMID: 10.1038/s41572-023-00490-x38272922)
Hotez PJ (2020) The rise or fall of neglected tropical diseases in East Asia Pacific. Acta Trop 202:105182. https://doi.org/10.1016/j.actatropica.2019.105182. (PMID: 10.1016/j.actatropica.2019.10518231550453)
Hotez PJ et al (2015) Neglected tropical diseases among the Association of Southeast Asian Nations (ASEAN): overview and update. PLoS Negl Trop Dis 9(4):e0003575. https://doi.org/10.1371/journal.pntd.0003575. (PMID: 10.1371/journal.pntd.0003575258807674400050)
Intapan PM, Maleewong W, Wongsaroj T, Singthong S, Morakote N (2005) Comparison of the quantitative formalin ethyl acetate concentration technique and agar plate culture for diagnosis of human strongyloidiasis. J Clin Microbiol 43(4):1932–1933. https://doi.org/10.1128/JCM.43.4.1932-1933.2005. (PMID: 10.1128/JCM.43.4.1932-1933.2005158150231081356)
Jung BK et al (2023) High endemicity of Opisthorchis viverrini infection among people in northern Cambodia confirmed by adult worm expulsion. Sci Rep 13(1):9654. https://doi.org/10.1038/s41598-023-36544-z. (PMID: 10.1038/s41598-023-36544-z3731667910267168)
Kaewpitoon N et al (2018) Detection of Opisthorchis viverrini Infection among the ASEAN Population in Thailand using a verbal screening test and fecal concentrator kit. Iran J Parasitol 13(2):258–266. (PMID: 300692106068376)
Keiser PB, Nutman TB (2004) Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev 17(1):208–217. https://doi.org/10.1128/CMR.17.1.208-217.2004. (PMID: 10.1128/CMR.17.1.208-217.200414726461321465)
Khieu V et al (2014a) High prevalence and spatial distribution of Strongyloides stercoralis in rural Cambodia. PLoS Negl Trop Dis 8(6):e2854. https://doi.org/10.1371/journal.pntd.0002854. (PMID: 10.1371/journal.pntd.0002854249216274055527)
Khieu V et al (2014b) Prevalence and risk factors of Strongyloides stercoralis in Takeo Province, Cambodia. Parasit Vectors 7:221. https://doi.org/10.1186/1756-3305-7-221. (PMID: 10.1186/1756-3305-7-221248867634029906)
Khuntikeo N et al (2015) Cohort profile: cholangiocarcinoma screening and care program (CASCAP). BMC Cancer 15:459. https://doi.org/10.1186/s12885-015-1475-7. (PMID: 10.1186/s12885-015-1475-7260544054459438)
Kramme S et al (2011) Novel real-time PCR for the universal detection of Strongyloides species. J Med Microbiol 60(Pt 4):454–458. https://doi.org/10.1099/jmm.0.025338-0. (PMID: 10.1099/jmm.0.025338-021163829)
Krolewiecki AJ et al (2018) Transrenal DNA-based diagnosis of Strongyloides stercoralis (Grassi, 1879) infection: Bayesian latent class modeling of test accuracy. PLoS Negl Trop Dis 12(6):e0006550. https://doi.org/10.1371/journal.pntd.0006550. (PMID: 10.1371/journal.pntd.0006550298567386007929)
Laoraksawong P et al (2018) Current high prevalences of Strongyloides stercoralis and Opisthorchis viverrini infections in rural communities in northeast Thailand and associated risk factors. BMC Public Health 18(1):940. https://doi.org/10.1186/s12889-018-5871-1. (PMID: 10.1186/s12889-018-5871-1300644076069555)
Mae AFW, Harriet W, Kirstin ER (2019) A review of strongyloides spp. environmental sources worldwide. Pathogens 8(3). https://doi.org/10.3390/pathogens8030091.
Minato K, Kimura E, Shintoku Y, Uga S (2008) Effect of temperature on the development of free-living stages of Strongyloides ratti. Parasitol Res 102(2):315–319. https://doi.org/10.1007/s00436-007-0773-7. (PMID: 10.1007/s00436-007-0773-718026994)
Ngern-klun R, Sukontason KL, Tesana S, Sripakdee D, Irvine KN, Sukontason K (2006) Field investigation of Bithynia funiculata, intermediate host of Opisthorchis viverrini in northern Thailand. Southeast Asian J Trop Med Public Health 37(4):662–672. (PMID: 17121291)
Phonekeo S et al (2023) Intestinal helminth infections and associated risk factors among adults in the Lao People’s Democratic Republic. Infect Dis Poverty 12(1):61. https://doi.org/10.1186/s40249-023-01112-0. (PMID: 10.1186/s40249-023-01112-03738652810311807)
Ruantip S et al (2019) Accuracy of urine and serum assays for the diagnosis of strongyloidiasis by three enzyme-linked immunosorbent assay protocols. Am J Trop Med Hyg 100(1):127–129. https://doi.org/10.4269/ajtmh.18-0569. (PMID: 10.4269/ajtmh.18-056930398144)
Saengsawang P, Promthet S, Bradshaw P (2012) Prevalence of OV infection in Yasothon Province, Northeast Thailand. Asian Pac J Cancer Prev 13(7):3399–3402. https://doi.org/10.7314/apjcp.2012.13.7.3399. (PMID: 10.7314/apjcp.2012.13.7.339922994767)
Sato Y, Kobayashi J, Shiroma Y (1995) Serodiagnosis of strongyloidiasis. The application and significance. Rev Inst Med Trop Sao Paulo 37(1):35–41. https://doi.org/10.1590/s0036-46651995000100006.
Schar F et al (2013) Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis 7(7):e2288. https://doi.org/10.1371/journal.pntd.0002288. (PMID: 10.1371/journal.pntd.0002288238750333708837)
Sithithaworn P et al (2003) Epidemiology of Strongyloides stercoralis in north-east Thailand: application of the agar plate culture technique compared with the enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 97(4):398–402. https://doi.org/10.1016/s0035-9203(03)90069-1. (PMID: 10.1016/s0035-9203(03)90069-115259466)
Sota P, Upontain S, Tangkawattana S, Punyapornwithaya V, Nakhapakorn K, Sripa B (2024) Association between Opisthorchis viverrini infection in cats and humans: non-spatial and spatial analyses. Vet Parasitol 327:110150. https://doi.org/10.1016/j.vetpar.2024.110150. (PMID: 10.1016/j.vetpar.2024.11015038422711)
Sripa B, Suwannatrai AT, Sayasone S, Do DT, Khieu V, Yang Y (2021) Current status of human liver fluke infections in the Greater Mekong Subregion. Acta Trop 224:106133. https://doi.org/10.1016/j.actatropica.2021.106133. (PMID: 10.1016/j.actatropica.2021.10613334509453)
Sripa B, Tangkawattana S, Sangnikul T (2017) The Lawa model: a sustainable, integrated opisthorchiasis control program using the EcoHealth approach in the Lawa Lake region of Thailand. Parasitol Int 66(4):346–354. https://doi.org/10.1016/j.parint.2016.11.013. (PMID: 10.1016/j.parint.2016.11.01327890720)
Suwannahitatorn P et al (2013) A follow-up study of Opisthorchis viverrini infection after the implementation of control program in a rural community, central Thailand. Parasit Vectors 6:188. https://doi.org/10.1186/1756-3305-6-188. (PMID: 10.1186/1756-3305-6-188237868633689608)
Suwannatrai A, Saichua P, Haswell M (2018) Epidemiology of Opisthorchis viverrini Infection. Adv Parasitol 101:41–67. https://doi.org/10.1016/bs.apar.2018.05.002. (PMID: 10.1016/bs.apar.2018.05.00229907255)
Suwannatrai AT et al (2021) Opisthorchis viverrini and Strongyloides stercoralis mono- and co-infections: Bayesian geostatistical analysis in an endemic area, Thailand. Acta Trop 223:106079. https://doi.org/10.1016/j.actatropica.2021.106079. (PMID: 10.1016/j.actatropica.2021.10607934363777)
Thinkhamrop K et al (2019) Repeated praziquantel treatment and Opisthorchis viverrini infection: a population-based cross-sectional study in northeast Thailand. Infect Dis Poverty 8(1):18. https://doi.org/10.1186/s40249-019-0529-5. (PMID: 10.1186/s40249-019-0529-5308901886425692)
Vonghachack Y, Sayasone S, Bouakhasith D, Taisayavong K, Akkavong K, Odermatt P (2015) Epidemiology of Strongyloides stercoralis on Mekong islands in southern Laos. Acta Trop 141(Pt B):289–294. https://doi.org/10.1016/j.actatropica.2014.09.016. (PMID: 10.1016/j.actatropica.2014.09.01625291044)
Wang YC, Yeo SP, Namsanor J, Sithithaworn P, Yang S (2022) Effects of environmental factors and infecting trematodes on the size and inorganic elements of bithynia siamensis goniomphalos snails in Northeast Thailand. Am J Trop Med Hyg 106(3):809–817. https://doi.org/10.4269/ajtmh.21-0038. (PMID: 10.4269/ajtmh.21-0038350080488922501)
Wattanawong O et al (2021) Current status of helminthiases in Thailand: a cross-sectional, nationwide survey, 2019. Acta Trop 223:106082. https://doi.org/10.1016/j.actatropica.2021.106082. (PMID: 10.1016/j.actatropica.2021.10608234364893)
Wharton-Smith A et al (2019) Gender-related factors affecting health seeking for neglected tropical diseases: findings from a qualitative study in Ethiopia. PLoS Negl Trop Dis 13(12):e0007840. https://doi.org/10.1371/journal.pntd.0007840. (PMID: 10.1371/journal.pntd.0007840318300266907747)
Wongratanacheewin S, Pumidonming W, Sermswan RW, Pipitgool V, Maleewong W (2002) Detection of Opisthorchis viverrini in human stool specimens by PCR. J Clin Microbiol 40(10):3879–3880. https://doi.org/10.1128/JCM.40.10.3879-3880.2002. (PMID: 10.1128/JCM.40.10.3879-3880.200212354909130907)
Worasith C et al (2015) Advances in the diagnosis of human Opisthorchiasis: development of Opisthorchis viverrini antigen detection in urine. PLoS Negl Trop Dis 9(10):e0004157. https://doi.org/10.1371/journal.pntd.0004157. (PMID: 10.1371/journal.pntd.0004157264850244618926)
Worasith C et al (2019) Comparing the performance of urine and copro-antigen detection in evaluating Opisthorchis viverrini infection in communities with different transmission levels in Northeast Thailand. PLoS Negl Trop Dis 13(2):e0007186. https://doi.org/10.1371/journal.pntd.0007186. (PMID: 10.1371/journal.pntd.0007186307354926383950)
Worasith C et al (2023) Long-term persistence of opisthorchis viverrini antigen in urine: a prospective study in Northeast Thailand. Am J Trop Med Hyg 108(2):356–358. https://doi.org/10.4269/ajtmh.22-0478. (PMID: 10.4269/ajtmh.22-047836572008)
Xu Y et al (2023) The prevalence of soil transmitted helminths and its influential factors in Shandong Province, China: an analysis of surveillance data from 2016 to 2020. Infect Dis Poverty 12(1):54. https://doi.org/10.1186/s40249-023-01100-4. (PMID: 10.1186/s40249-023-01100-43721795610201724)

IN63270 Invitation Research Fund, Faculty of Medicine, Khon Kaen University, Thailand; IN63270 Invitation Research Fund, Faculty of Medicine, Khon Kaen University, Thailand

Keywords: Opisthorchis viverrini; Strongyloides stercoralis; Prevalence; Risk factors; Thailand

Date Created: 20241223 Date Completed: 20241223 Latest Revision: 20241223

20241223

10.1007/s00436-024-08427-3

39714601