Uncovering the Pathogenic Landscape of Helminth (Opisthorchis viverrini) Infections: A Cross-Sectional Study on Contributions of Physical and Social Environment and Healthcare Interventions.

Xueyuan Ong,David Taylor,Yi-Chen Wang,Luxana Laithavewat,Paiboon Sithithaworn,Jutamas Namsanor,Song Liang

doi:10.1371/journal.pntd.0005175

Xueyuan Ong, David Taylor + Show 5 more

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https://doi.org/10.1371/journal.pntd.0005175

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Abstract

BackgroundHelminth infections have proven recalcitrant to control by chemotherapy in many parts of Southeast Asia and indeed farther afield. This study isolates and examines the influence of different aspects of the physical and social environment, and uneven intervention effort contributing to the pathogenic landscape of human Opisthorchis viverrini infections.MethodologyA cross-sectional survey, involving 632 participants, was conducted in four villages in northeast Thailand to examine the impact on prevalence and parasite burden of the reservoir dam environment, socio-economic, demographic, and behavioral factors, and health center intervention efforts. Formalin-ether concentration technique was used for diagnoses, and multivariate models were used for analyses.Principal FindingsThe importance attributed to O. viverrini infections varied among health centers in the four study villages. Villages where O. viverrini infections were not prioritized by the health centers as the healthcare focus were at a higher risk of infection (prevalence) with odds ratio (risk factor) of 5.73 (3.32–10.27) and p-value < 0.01. Priority of healthcare focus, however, did not appear to influence behavior, as the consumption of raw fish, the main source of O. viverrini infections in the study area, was 11.4% higher in villages that prioritized O. viverrini infections than those that did not (p-value = 0.01). Landscape variation, notably proximity to reservoir, affects vulnerability of local population to infection. Infection intensity was higher in population located closer to the reservoir with risk ratio of 2.09 (1.12–4.02) and p-value < 0.01. Patterns of infection intensities among humans were found to match fish infection intensity, where higher infection intensities were associated with fish obtained from the reservoir waterbody type (p-value = 0.023).Conclusions/SignificanceThis study demonstrated the importance of environmental influence and healthcare focus as risk factors of infections in addition to the socio-economic, demographic, and behavioral factors commonly explored in existing studies. The reservoir was identified as a crucial source to target for opisthorchiasis intervention efforts and the need to consider infection intensity in disease control efforts was highlighted. The holistic approach in this study, which underscores the close relationship between the environment, animals, and humans in development of human infections or diseases, is an important contribution to the framework of One Health approach, where consideration of helminth diseases has largely been overlooked.

Highlights

Helminthiases, which include foodborne trematodiases, lymphatic filariasis, schistosomiasis, and soil-transmitted helminthiases, are the most common neglected tropical diseases (NTDs) in southeast Asia [1]
Comparison of the O. viverrini infection prevalence and intensity of the four villages showed that the S-river village had the highest prevalence at 40.21%, while the N-reservoir village had the highest infection intensity at 99.41 epg (Fig 2A)
When villages were grouped according to their proximity to waterbody types, infection prevalence did not vary much between villages located close to the reservoir and to the river inlets, but infection intensity was significantly higher for the reservoir villages at 93.72 epg than for the river villages at 38.54 epg

Summary

Introduction

Helminthiases, which include foodborne trematodiases, lymphatic filariasis, schistosomiasis, and soil-transmitted helminthiases, are the most common neglected tropical diseases (NTDs) in southeast Asia [1] They disproportionally affect the poor or marginalized population in developing countries, trapping the afflicted in a vicious cycle of poor health outcomes and poverty, and costing billions of dollars in treatment each year [2]. The increasing recognition of the burden caused by helminth infections has brought about large-scale control programs by the World Health Organization and other nationwide control programs in countries in Asia [3,4], Latin America [5], and sub-Saharan Africa [6], where helminthiases are prevalent These programs have primarily relied upon chemotherapy for helminthiases control [7]. This study isolates and examines the influence of different aspects of the physical and social environment, and uneven intervention effort contributing to the pathogenic landscape of human Opisthorchis viverrini infections

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Discussion

Conclusion