Soil-Transmitted Helminth infections reduction in Bhutan: A report of 29 years of deworming

Autoři: Tshering Dukpa aff001;  Nidup Dorji aff001;  Sangay Thinley aff002;  Wangchuk aff001;  Karma Tshering aff003;  Kinley Gyem aff004;  Diki Wangmo aff001;  Passang Lhamo Sherpa aff001;  Tshering Dorji aff005;  Antonio Montresor aff006
Působiště autorů: Faculty of Nursing and Public Health, Khesar Gyalpo University of Medical Sciences of Bhutan, Thimphu, Bhutan aff001;  Comprehensive School Health Programme, Department of Public Health, Ministry of Health, Thimphu, Bhutan aff002;  Department of Microbioloy, Jigme Dorji Wangchuk National Referral Hospital, Thimphu, Bhutan aff003;  Royal Center for Disease Control, Thimphu Bhutan aff004;  Laboratory Unit, Trashigang District Hospital, Trashigang, Bhutan aff005;  Department of Control of Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland aff006
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227273


Soil Transmitted Helminth (STH) infections affect over 1.5 billion people worldwide. Although prevalent in all age groups, school aged children are a high-risk groups for STH infections. In Bhutan, epidemiological data on STH were collected from western Bhutan in 2003, which found a prevalence of 16.5%. However, little evidence is available on the prevalence of infection at national level. Therefore, this study was conducted with the aim to assess the prevalence and intensity of STH infections, and identify significant correlates of STH among students. A school-based survey was conducted in three regions of Bhutan. Two-stage cluster sampling was adopted to select a sample of 1500 students from 24 schools, in equal proportion from three regions of the country. A total of 1456 (97%) students were interviewed and their stool sample examined for the presence of parasites. Mini-FLOTAC technique was used to detect the parasite eggs/ova. The prevalence of any STH infection was 1.4%, with 0.8% Ascaris lumbricoides, 0.5% Trichuris trichiura and 0.2% hookworms. The eastern region had the highest prevalence at 2.3%. Except for one student who had moderate intensity of A. lumbricoides, the rest had light infection. Any STH presence was significantly associated with father’s occupation, father’s education level, type of house and the flooring of the house in which students reported to live. No significant associations were observed between water, sanitation and hygiene (WASH) variables measured and presence of any STH infection. The prevalence of STH was found to be very low with primarily light intensity in this study. Nonetheless, it was also found that the sanitation situation is not ideal in the country, with several students reporting constant or partial open defecation leading to environmental contamination. Based on this prevalence and in line with the WHO guideline, it is recommended that deworming be reduced to once a year in combination with concerted health education on proper hygiene and sanitation practice.

Klíčová slova:

Fathers – Helminth infections – Hygiene – Sanitation – Schools – Water resources – Soil-transmitted helminthiases – Bhutan


1. 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 medicine. 2014;11(3):e1001620. doi: 10.1371/journal.pmed.1001620 24667810

2. World Health Organization. Water sanitation & hygiene for accelerating and sustaining progress on neglected tropical diseases: a global strategy 2015–2020. 2015.

3. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet. 2006;367(9521):1521–32.

4. Horton J. Human gastrointestinal helminth infections: are they now neglected diseases? Trends in parasitology. 2003;19(11):527–31. doi: 10.1016/ 14580965

5. Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. The Lancet. 2017.

6. World Health Organization. Helminth control in school-age children: a guide for managers of control programmes: World Health Organization; 2011.

7. World Health Organization. Fact Sheet-Soil-transmitted helminth infections 2017 [updated 20 February 2018; cited 2018 25 March ].

8. Ziegelbauer K, Speich B, Mausezahl D, Bos R, Keiser J, Utzinger J. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med. 2012;9(1):e1001162. doi: 10.1371/journal.pmed.1001162 22291577

9. World Health Organization. Eliminating soil-transmitted Helminthiases as a public health problem in children: progress report 2001–2010 and strategic plan 2011–2020. 2012.

10. Taylor-Robinson DC, Maayan N, Soares-Weiser K, Donegan S, Garner P. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin, and school performance. The Cochrane database of systematic reviews. 2015(7):CD000371–CD. doi: 10.1002/14651858.CD000371.pub6 26202783

11. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, et al. Soil transmitted helminths and schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. BMC infectious diseases. 2011;11(1):189–.

12. Campbell SJ, Savage GB, Gray DJ, Atkinson J-AM, Magalhaes RJS, Nery SV, et al. Water, sanitation, and hygiene (WASH): a critical component for sustainable soil-transmitted helminth and schistosomiasis control. PLoS neglected tropical diseases. 2014;8(4):e2651. doi: 10.1371/journal.pntd.0002651 24722335

13. Allen H, Sithey G, Padmasiri EA, Montresor A. Epidemiology of soil-transmitted helminths in the western region of Bhutan. The Southeast Asian journal of tropical medicine and public health. 2004;35(4):777–9. 15916067

14. Patil SR, Arnold BF, Salvatore AL, Briceno B, Ganguly S, Colford JM Jr., et al. The effect of India's total sanitation campaign on defecation behaviors and child health in rural Madhya Pradesh: a cluster randomized controlled trial. 2014(1549–1676 (Electronic)).

15. Benjamin-Chung J, Nazneen A, Halder AK, Haque R, Siddique A, Uddin MS, et al. The Interaction of Deworming, Improved Sanitation, and Household Flooring with Soil-Transmitted Helminth Infection in Rural Bangladesh. PLoS Neglected Tropical Diseases. 2015;9(12):e0004256–e. doi: 10.1371/journal.pntd.0004256 26624994

16. Barda BD, Rinaldi L, Ianniello D, Zepherine H, Salvo F, Sadutshang T, et al. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Negl Trop Dis. 2013;7(8):e2344–pe. doi: 10.1371/journal.pntd.0002344 23936577

17. Barda B, Zepherine H, Rinaldi L, Cringoli G, Burioni R, Clementi M, et al. Mini-FLOTAC and Kato-Katz: helminth eggs watching on the shore of Lake Victoria. Parasites & vectors. 2013;6(1):220–.

18. World Health Organization. Assessing the epidemiology of soil-transmitted helminths during a transmission assessment survey in the global programme for the elimination of lymphatic filariasis. World Health Organization, 2015.

19. Assefa LM, Crellen T, Kepha S, Kihara JH, Njenga SM, Pullan RL, et al. Diagnostic accuracy and cost-effectiveness of alternative methods for detection of soil-transmitted helminths in a post-treatment setting in western Kenya. (1935–2735 (Electronic)).

20. Kunwar R, Acharya L, Karki S. Trends in prevalence of soil-transmitted helminth and major intestinal protozoan infections among school-aged children in Nepal. Tropical Medicine and International Health. 2016;21(1365–3156 (Electronic)).

21. Ganguly S, Barkataki S, Karmakar S, Sanga P, Boopathi K, Kanagasabai K, et al. High prevalence of soil-transmitted helminth infections among primary school children, Uttar Pradesh, India, 2015. Infectious Diseases of Poverty. 2017(2049–9957 (Electronic)).

22. Sanchez AL, Gabrie JA, Usuanlele M-T, Rueda MM, Canales M, Gyorkos TW. Soil-transmitted helminth infections and nutritional status in school-age children from rural communities in Honduras. PLoS neglected tropical diseases. 2013;7(8):e2378–e. doi: 10.1371/journal.pntd.0002378 23951385

23. Ranjan S, Passi SJ, Singh SN. Prevalence and risk factors associated with the presence of Soil-Transmitted Helminths in children studying in Municipal Corporation of Delhi Schools of Delhi, India. Journal of Parasitic Diseases. 2015(0971–7196 (Print)).

24. Kattula D Fau—Sarkar R, Sarkar R Fau—Rao Ajjampur SS, Rao Ajjampur Ss Fau—Minz S, Minz S Fau—Levecke B, Levecke B Fau—Muliyil J, Muliyil J Fau—Kang G, et al. Prevalence & risk factors for soil transmitted helminth infection among school children in south India. Indian Journal of Medical Research. 2014;139(1(Print)):76–82. 24604041

25. Kirwan P, Asaolu So Fau—Abiona TC, Abiona Tc Fau—Jackson AL, Jackson Al Fau—Smith HV, Smith Hv Fau—Holland CV, Holland CV. Soil-transmitted helminth infections in Nigerian children aged 0–25 months. (1475–2697 (Electronic)).

26. Salawu SA, Ughele VA. Prevalence of soil-transmitted helminths among school-age children in Ife East Local Government Area, Osun State, Nigeria. FUTA Journal of Research in Sciences. 2015;11:139–51.

27. Wang X, Zhang L, Luo R, Wang G, Chen Y, Medina A, et al. Soil-transmitted helminth infections and correlated risk factors in preschool and school-aged children in rural southwest China. PLoS One. 2012;7(9):e45939. doi: 10.1371/journal.pone.0045939 23029330

28. Greenland K, Dixon R, Khan SA, Gunawardena K, Kihara JH, Smith JL, et al. The Epidemiology of Soil-Transmitted Helminths in Bihar State, India. PLoS Neglected Tropical Diseases. 2015;9(5):e0003790–e. doi: 10.1371/journal.pntd.0003790 25993697

29. Shumbej T, Belay T, Mekonnen Z, Tefera T, Zemene E. Soil-Transmitted Helminths and Associated Factors among Pre-School Children in Butajira Town, South-Central Ethiopia: A Community-Based Cross-Sectional Study. PloS one. 2015;10(8):e0136342. doi: 10.1371/journal.pone.0136342 26305361

30. Knopp S, Mgeni Af Fau—Khamis IS, Khamis Is Fau—Steinmann P, Steinmann P Fau—Stothard JR, Stothard Fau—Rollinson D Jr, Rollinson D Fau—Marti H, et al. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. (1935–2735 (Electronic)).

31. Dreyer G, Fernandes-Silva E, Alves S, Rocha A, Albuquerque R, Addiss D. Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. Journal of clinical microbiology. 1996;34(10):2569–71. 8880521

32. Montresor A, Mupfasoni D. Achievements of the deworming programme in Sri Lanka. (2214–109X (Electronic)).

33. Safi N, Warusavithana S, Alawi SAS, Atta H, Montresor A, Gabrielli AF. Elimination of morbidity due to soil-transmitted helminthiases among Afghan schoolchildren. Acta tropica. 2019;197:105035. doi: 10.1016/j.actatropica.2019.05.026 31128094

34. Casey GJ, Tinh TT, Tien NT, Hanieh S, Cavalli-Sforza LT, Montresor A, et al. Sustained effectiveness of weekly iron-folic acid supplementation and regular deworming over 6 years in women in rural Vietnam. PLoS neglected tropical diseases. 2017;11(4):e0005446. doi: 10.1371/journal.pntd.0005446 28406909

35. Tun A, Myat SM, Gabrielli AF, Montresor A. Control of soil‐transmitted helminthiasis in M yanmar: results of 7 years of deworming. Tropical Medicine & International Health. 2013;18(8):1017–20.

36. Phommasack B, Saklokham K, Chanthavisouk C, Nakhonesid-Fish V, Strandgaard H, Montresor A, et al. Coverage and costs of a school deworming programme in 2007 targeting all primary schools in Lao PDR. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2008;102(12):1201–6. doi: 10.1016/j.trstmh.2008.04.036 18554674

37. Montresor A, Trouleau W, Mupfasoni D, Bangert M, Joseph S, Mikhailov A, et al. Preventive chemotherapy to control soil-transmitted helminthiasis averted more than 500 000 DALYs in 2015. Transactions of The Royal Society of Tropical Medicine and Hygiene. 2017;111(10):457–63. doi: 10.1093/trstmh/trx082 29346640

38. Passerini L, Casey GJ, Biggs BA, Cong DT, Phu LB, Phuc TQ, et al. Increased birth weight associated with regular pre-pregnancy deworming and weekly iron-folic acid supplementation for Vietnamese women. PLoS neglected tropical diseases. 2012;6(4):e1608. doi: 10.1371/journal.pntd.0001608 22509421

39. Mupfasoni DA-Ohoo, Bangert M, Mikhailov A, Marocco C, Montresor A. Sustained preventive chemotherapy for soil-transmitted helminthiases leads to reduction in prevalence and anthelminthic tablets required. (2049–9957 (Electronic)).

Článek vyšel v časopise


2020 Číslo 1