Prevalence and risk factors of soil transmitted helminth infections among school-aged children in Garut, Indonesia: Insights from a six-year deworming intervention

Abstract

Objective: To assess prevalence and factors associated with soil-transmitted helminth (STH) infections among rural school children.

Methods: This school-based survey applied a cross-sectional design which included children aged 6-14 years enrolled in 12 elementary schools in Banjarwangi, Garut, West Java Province. Stool and blood samples were collected from 388 randomly selected students to examine the STH infections and anemia status, respectively. Anthropometric assessment was performed to profile nutritional status. A structured questionnaire was employed to collect socio-demographic and school performance data. Multivariable logistic regression models were built to assess the factors associated with STH infections in school children.

Results: Among 386 schoolchildren, 9.8% children were positive for one or more STH infections, predominantly Trichuris trichiura (9.0%), with males (n=23), significantly more infected than females (n=13) (5.9% vs. 3.4%, P=0.04). The most infected age group was 6-10 years (n=25, 6.5%). The prevalence of STH infection was significantly higher among students that practicing open defecation (n=22, 5.7%) (P=0.03). The odds risk of STH infections was associated with practicing open defecation (aOR 2.54, 95% CI 1.17-5.53, P=0.02).

Conclusions: The findings from this study demonstrate the persistent STH transmission among children underscoring the need for sustained post-MDA intervention strategies in resource-limited settings.

Keywords

Soil-transmitted helminths / School-age children / Academic performance / Stunted / Open defecation

References

[1] Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: Ascariasis, trichuriasis, and hookworm. Lancet 2006; 367(9521): 1521-1532.

[2] World Health Organization. Soil-transmitted helminthiasis. World Health Organization 2012. [Online]. Available from: https://iris.who.int/bitstream/handle/10665/44804/97892415%2003129_eng.pdf?sequence=1. [Accessed on 25 January 2024].

[3] Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 2014; 7: 37. doi: 10.1186/1756-3305-7-37.

[4] Liu C, Luo R, Yi H, Zhang L, Li S, Bai Y, et al. Soil-transmitted helminths in Southwestern China: A cross-sectional study of links to cognitive ability, nutrition, and school performance among children. PLoS Negl Trop Dis 2015; 9(6): e0003877. doi: 10.1371/journal.pntd.0003877.

[5] Fauziah N, Ar-Rizqi MA, Hana S, Patahuddin NM, Diptyanusa A. Stunting as a risk factor of soil-transmitted helminthiasis in children: A literature review. Interdiscip Perspect Infect Dis 2022; Aericle ID: 8929025. doi: 10.1155/2022/8929025. eCollection 2022.

[6] Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: A systematic review and meta-analysis. PLoS Med 2014; 11(3): e1001620. doi: 10.1371/journal.pmed.1001620.

[7] Ngure FM, Reid BM, Humphrey JH, Mbuya MN, Pelto G, Stoltzfus RJ. Water, sanitation, and hygiene (WASH), environmental enteropathy, nutrition, and early child development: Making the links. Ann N Y Acad Sci 2014; 1308(1): 118-128.

[8] Null C, Stewart CP, Pickering AJ, Dentz HN, Arnold BF, Arnold CD, et al. Effects of water quality, sanitation, handwashing, and nutritional interventions on diarrhoea and child growth in rural Kenya: A cluster-randomised controlled trial. Lancet Glob Heal 2018; 6(3): e316-e329.

[9] Clasen T, Boisson S, Routray P, Torondel B, Bell M, Cumming O, et al. Effectiveness of a rural sanitation programme on diarrhoea, soil-transmitted helminth infection, and child malnutrition in Odisha, India: A cluster-randomised trial. Lancet Glob Heal 2014; 2(11): e645-e653.

[10] Ercumen A, Benjamin-Chung J, Arnold BF, Lin A, Hubbard AE, Stewart C, et al. Effects of water, sanitation, handwashing and nutritional interventions on soil-transmitted helminth infections in young children: A cluster-randomized controlled trial in rural Bangladesh. PLoS Negl Trop Dis 2019; 3(5): e0007323.

[11] Sakti H, Nokes C, Hertanto WS, Hendratno S, Hall A, Bundy DAP, et al. Evidence for an association between hookworm infection and cognitive function in Indonesian school children. Trop Med Int Heal 1999; 4(5): 322-334.

[12] Chard AN, Garn JV, Chang HH, Clasen T, Freeman MC. Impact of a school-based water, sanitation, and hygiene intervention on school absence, diarrhea, respiratory infection, and soil-transmitted helminths: Results from the WASH HELPS cluster-randomized trial. J Glob Health 2019; 9(2): 020402. doi: 10.7189/jogh.09.020402.

[13] Belachew A, Tewabe T. Under-five anemia and its associated factors with dietary diversity, food security, stunted, and deworming in Ethiopia: Systematic review and meta-analysis. Syst Rev 2020; 9(1): 31. doi: 10.1186/s13643-020-01289-7.

[14] World Health Organization. Neglected tropical diseases-prevention, control, elimination and eradication. WHA 66.20. Sixty-Sixth World Heal Assem 2013. [Online]. Available from: https://apps.who.int/gb/ebwha/pdf_files/WHA66/A66_20-en.pdf. [Accessed on 4 February 2024].

[15] West Java Province. DKP Garut Beri Bantuan Pangan Untuk Penanganan Stunting di Kecamatan Banjarwangi. [Online]. Available from: https://jabarprov.go.id/berita/dkp-garut-beri-bantuan-pangan-untuk-penanganan-stunting-di-kecamatan-banjarwangi-2471. [Accessed on 13 June 2024].

[16] Provincial Statistics Bureau. Provinsi Jawa Barat Dalam Angka 2023. [Online]. Available from: https://jabar.bps.go.id/publication/2023/02/28/57231a828abbfdd50a21fe31/provinsi-jawa-barat-dalam-angka-2023.html. [Accessed on 4 May 2024].

[17] Speich B, Knopp S, Mohammed KA, Khamis IS, Rinaldi L, Cringoli G, et al. Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasit Vectors 2010;3(1). doi: 10.1186/1756-3305-3-71.

[18] World Health Organization. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Geneva; 2011. [Online]. Available from: https://www.who.int/publications/i/item/WHO-NMH-NHD-MNM-11.1. [Accessed on 10 January 2023].

[19] World Health Organization. Multicentre Growth Reference Study Group: WHO Child Growth Standards based on length/height, weight and age. Acta Paediatr Suppl 2006; 450: 76-85. doi: 10.1111/j.1651-2227.2006.tb02378.x.

[20] World Health Organization. AnthroPlus software. [Online]. Available from: https://www.who.int/tools/growth-reference-data-for-5to19-years/application-tools. [Accessed on 10 January 2023].

[21] Bursac Z, Gauss CH, Williams DK, Hosmer DW. Purposeful selection of variables in logistic regression. Source Code Biol Med 2008; 3: 17.

[22] Labana R, Romero V, Guinto A, Caril A, Untalan K, Reboa A, et al. Prevalence and intensity of soil-transmitted helminth infections among school-age children in the Cagayan Valley, the Philippines. Asian Pac J Trop Med 2021; 14(3): 113-121.

[23] Rosa BA, Supali T, Gankpala L, Djuardi Y, Sartono E, Zhou Y, et al. Differential human gut microbiome assemblages during soil-transmitted helminth infections in Indonesia and Liberia. Microbiome 2018; 6(1): 33.

[24] Wandra T, Darlan DM, Yulfi H, Purba IE, Sato MO, Budke CM, et al. Soil-transmitted helminth infections and taeniasis on Samosir Island, Indonesia. Acta Trop 2020; 202: 105250. doi: 10.1016/j.actatropica.2019.105250.

[25] Nasution RKA, Nasution BB, Lubis M, Lubis IND. Prevalence and knowledge of soil-transmitted helminth infections in Mandailing Natal, North Sumatera, Indonesia. Open Access Maced J Med Sci 2019; 7(20): 3443-3346.

[26] Grau-Pujol B, Gandasegui J, Escola V, Marti-Soler H, Cambra-Pellejà M, Demontis M, et al. Single-nucleotide polymorphisms in the beta-tubulin gene and its relationship with treatment response to albendazole in human soil-transmitted helminths in Southern Mozambique. Am J Trop Med Hyg 2022; 107(3): 649-657.

[27] Hürlimann E, Keller L, Patel C, Welsche S, Hattendorf J, Ali SM, et al. Efficacy and safety of co-administered ivermectin and albendazole in school-aged children and adults infected with Trichuris trichiura in Côte d’Ivoire, Laos, and Pemba Island, Tanzania: A double-blind, parallel-group, phase 3, randomised controlled trial. Lancet Infect Dis 2022; 22(1): 123-135.

[28] Zeynudin A, Degefa T, Tesfaye M, Suleman S, Yesuf EA, Hajikelil Z, et al. Prevalence and intensity of soil-transmitted helminth infections and associated risk factors among household heads living in the peri-urban areas of Jimma town, Oromia, Ethiopia: A community-based cross-sectional study. PLoS One 2022; 17(9): e0274702.

[29] Getaneh Z, Enawgaw B, Engidaye G, Seyoum M, Berhane M, Abebe Z, et al. Prevalence of anemia and associated factors among school children in Gondar town public primary schools, northwest Ethiopia: A school-based cross-sectional study. PLoS One 2017; 12(12): e0190151. doi: 10.1371/journal.pone.0190151. eCollection 2017.

[30] Kache R, Phasuk N, Viriyavejakul P, Punsawad C. Prevalence of soil-transmitted helminth infections and associated risk factors among elderly individuals living in rural areas of southern Thailand. BMC Public Health 2020; 20(1): 1882. doi: 10.1186/s12889-020-09986-7.

[31] Farrant O, Marlais T, Houghton J, Goncalves A, Teixeira da Silva Cassama E, Cabral MG, et al. Prevalence, risk factors and health consequences of soil-transmitted helminth infection on the Bijagos Islands, Guinea Bissau: A community-wide cross-sectional study. PLoS Negl Trop Dis 2020; 14(12): e0008938.

[32] Ihnacik L, Šmigová J, Šoltys J, Bobíková D, Kuzevičová Ž, Kuzevič Š, et al. The survey of soil-transmitted helminth species abundance in Slovakia with an emphasis on parameters important for their distribution. Front Med 2022; 9: 1043313.

[33] Fauziah N, Aviani JK, Agrianfanny YN, Fatimah SN. Intestinal parasitic infection and nutritional status in children under five years old: A systematic review. Trop Med Infect Dis 2022; 7(11): 371. doi: 10.3390/tropicalmed7110371.

[34] Alnaz ARM, Darlan DM, Andriyani Y, Lubis RR. Hemoglobin level and risk of anemia in soil-transmitted helminths infections among children: A systematic review and meta-analysis. Open Access Maced J Med Sci 2022; 10(F): 355-363.

[35] Zeng W, Malla P, Xu X, Pi L, Zhao L, He X, et al. Associations among soil-transmitted helminths, G6PD deficiency and asymptomatic malaria parasitemia, and anemia in schoolchildren from a conflict zone of northeast Myanmar. Am J Trop Med Hyg 2020; 102(4): 851-856.

[36] Suraweera O, Galgamuwa L, Wickramasinghe S, Iddawela D, Nandasiri N. Soil-transmitted helminth infections, associated factors and nutritional status in an estate community in Sri Lanka. Sri Lankan J Infect Dis 2018; 8(2): 100.

[37] Utzinger J, Bergquist R, Olveda R, Zhou XN. Important helminth infections in southeast Asia. Diversity, potential for control and prospects for elimination. Adv Parasitol 2010:72:1-30. doi: 10.1016/S0065-308X(10)72001-7.

[38] Landeryou T, Maddren R, Gomez SR, Kalahasti S, Liyew EF, Chernet M, et al. Longitudinal monitoring of prevalence and intensity of soil-transmitted helminth infections as part of community-wide mass drug administration within the Geshiyaro project in the Bolosso Sore district, Wolaita, Ethiopia. PLoS Negl Trop Dis 2022; 16(9): e0010408. doi: 10.1371/journal.pntd.0010408.

[39] Dunn JC, Bettis AA, Wyine NY, Lwin AMM, Tun A, Maung NS, et al. Soil-transmitted helminth reinfection four and six months after mass drug administration: Results from the delta region of Myanmar. PLoS Negl Trop Dis 2019; 13(2): e0006591. doi: 10.1371/journal.pntd.0006591.

[40] Ngwese MM, Manouana GP, Moure PAN, Ramharter M, Esen M, Adégnika AA. Diagnostic techniques of soil-transmitted helminths: Impact on control measures. Trop Med & Infect Dis 2020; 5(2): 93.