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Clinical Helminthiases in Thailand Border Regions Show Elevated

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Clinical Helminthiases in Thailand Border Regions Show Elevated Adisakwattana et al. Parasites Vectors (2020) 13:416 https://doi.org/10.1186/s13071-020-04290-0 Parasites & Vectors RESEARCH Open Access Clinical helminthiases in Thailand border regions show elevated prevalence levels using qPCR diagnostics combined with traditional microscopic methods Poom Adisakwattana1*, Tippayarat Yoonuan1, Orawan Phuphisut1, Akkarin Poodeepiyasawat1, Nirundorn Homsuwan1, Catherine A. Gordon2, Donald P. McManus2, Louise E. Atkinson3, Angela Mousley3 and Geofrey N. Gobert3* Abstract Background: Under-regulated national borders in Southeast Asia represent potential regions for enhanced parasitic helminth transmission and present barriers to helminthiasis disease control. Methods: Three Thailand border regions close to Myanmar, Laos and Cambodia were surveyed for clinical parasitic helminth disease. In-feld microscopy was performed on stools from 567 individuals. Sub-samples were transported to Bangkok for molecular analysis comprising three multiplex qPCR assays. Results: The overall helminth infection prevalence was 17.99% as assessed by Kato-Katz and 24.51% by qPCR. The combined prevalence of the two methods was 28.57%; the most predominant species detected were Opisthorchis viverrini (18.34%), hookworm (6.88%; Ancylostoma spp. and Necator americanus), Ascaris lumbricoides (2.29%) and Trichuris trichiura (1.76%). Conclusions: These data demonstrate the value of molecular diagnostics for determining more precise prevalence levels of helminthiases in Southeast Asia. Availability of such accurate prevalence information will help guide future public health initiatives and highlights the need for more rigorous surveillance and timely intervention in these regions. Keywords: Helminthiases, Kato-Katz, molecular diagnostics, qPCR, Thailand border regions, Southeast Asia Background one third of cases occurring in Southeast Asia [2]. Most Parasitic worm infections (helminthiases) of humans afected are young people, particularly pre- and primary greatly impact low to medium income countries, includ- school-aged children (0–12 years), leading to a range ing Tailand and bordering countries. Worldwide, hel- of health issues including stunted growth and delayed minths infect an estimated 1.45 billion people [1], with mental development [3]. Since most helminth diseases cause chronic morbidity (95% of health-attributed losses) *Correspondence: [email protected]; [email protected] rather than acute disease, the impact on the health and 1 Department of Helminthology, Faculty of Tropical Medicine, Mahidol economic output of endemic areas is frequently reported University, Bangkok 10400, Thailand 3 in terms of disability-adjusted life years (DALYS); these School of Biological Sciences, Queenʼs University Belfast, Belfast BT9 5DL, UK measure the years lost due to morbidity, illness, and pre- Full list of author information is available at the end of the article mature death. Helminth infections worldwide in 2010 © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea- tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo- main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Adisakwattana et al. Parasites Vectors (2020) 13:416 Page 2 of 10 were responsible for 14 million DALYs [4]. Hookworm provinces of Sisaket, Tak and Ubon Ratchathani (Fig. 1). Te infection alone, largely due to anaemia, was responsible spots marked in the enlarged panels in the Fig. 1 represent for over 4 million DALYs, with the total economic loss individual houses normally located in clusters and distribute due to reduced productivity estimated to be between across several village. Within these provinces a total of 14 US$7.5–138.9 billion [5]. villages were surveyed (7, 1 and 6, respectively). Te results Helminth infections are routinely feld diagnosed using from the two diagnostic approaches have been reported to the “gold standard” Kato-Katz (KK) method, a low-sensi- health promoting hospitals in the targeted areas for further tivity microscopic technique, which is limited by species action by local medical doctors or heath ofcers according range and quantitative accuracy. Te KK can underesti- to treatment guidelines provided by the Department of Dis- mate prevalence [6] and therefore impact on MDA (mass ease Control, Ministry of Public Health, Tailand [12]. drug administration) programmes and outcomes. Te previous national surveillance on intestinal hel- Sample collection minthiases in Tailand, conducted by the Tai Ministry Te three feld sites were visited on one occasion each of Public Health in 2009, revealed an overall prevalence between December 2017 and February 2018. In the 14 (among 15,555 Tai people) of 18.1% with the highest villages surveyed, 567 clinical faecal samples were col- prevalence in the North-eastern region of Tailand [7]. lected. Across the Sisaket and Ubon Ratchathani sites 200 Recently, only limited spatial and temporal surveillance faecal samples from both provinces were collected (400 has been conducted, which may be insufcient to ade- in total) and 167 were collected from the Tak site. Ages of quately guide the national public health initiatives [8–10]. participants (311 females; 256 males) ranged from 1.5 to Moreover, helminth prevalence surveillance studies car- 88 years; age demographic data were not collected for 43 ried out to date [7, 9, 11] have been undertaken primarily sampled individuals. using microscopy-based faecal examination (KK) without Labelled sample cups were provided to health volun- combining with molecular detection, which may under- teers for distribution to participants. Te samples were estimate the actual extent of helminth infection. collected the next day either by health volunteers or In this study we explore the utility of molecular diag- brought to a collection point by participants. Informa- nostic procedures for the detection of active helminth tion on age, gender, occupation, and geographical loca- disease in Tai populations close to border regions with tion, was collected at the same time as faecal samples. KK Myanmar, Laos and Cambodia. Comparisons with the analysis was conducted at the site. Parallel faecal samples traditional KK microscopy are made and the strengths were stored in 80% (v/v) ethanol for transport at ambient and weakness of both methods assessed and discussed. temperature to Bangkok for molecular analysis. Te central aim of this work was to provide a more accu- KK was performed on all human faecal samples col- rate picture of the prevalence of helminthiases in these lected as previously reported [13–15]. In brief, individual areas. With this key information public health ofcials stool samples were pressed through a stainless sieve (size will be able to better plan control measures for the future 40 mesh: 420 µm sieve opening), and the non-retained to reduce helminth disease transmission. material used to fll a kit template which equated to 39.2 mg of material. Glycerin-malachite green-soaked cel- Methods lophane was placed on the sample with a glass slide and Study areas frmly pressed to spread the stool evenly across the sur- All study sites were located near three Tai border regions face. Te slide was viewed on a light microscope after Villages within these border regions were surveyed (Fig. 1): 30 min. Two slides were prepared from each sample and (i) the Mae Song Sub-District, Tasongyang District and analysed independently by two trained microscopists. All Tak Province close to the Tai-Myanmar border; (ii) Kham eggs were identifed as observed when possible. All sam- Khuean Kaeo Sub-District of Sirindhorn District within ples were anonymised and analysed blinded. Ubon Ratchathani Province at the Tai-Lao border; and (iii) the Phran Sub-District of Khun Han District in Sisa- Multiplex qPCR ket Province at close proximity to the Tai-Cambodia Due to the breadth of the potential helminth infection border. Based on annual income per person per year, the profle amongst the participants, this study screened for regions surveyed in Tak Province are considered to be 9 helminth species. As a result, three separate multiplex of low socioeconomic status, while those in Srisaket and PCR assays were developed to identify the presence of Ubonratchathani Provinces are considered to be of middle helminth DNA in faecal samples. Faecal DNA was iso- socioeconomic status. All study sites were located within lated using QIAamp® Fast DNA Stool Mini Kit (Qiagen Tailand but were close (1–10 km) to the bordering coun- GmbH, Hilden, Germany). A 1% agarose/TAE electropho- tries. Te three sites included multiple villages within the resis gel was used to check all samples after faecal DNA Adisakwattana
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