Abstract
Enterobiasis is a highly infectious parasitic disease spreading worldwide including Yemen. Therefore, this study aimed to investigate the prevalence and risk factors of enterobiasis among Yemeni children in Dhamar governorate. A total of 402 children (aged 1–12 years) participated in this cross-sectional survey carried out at Thamar University Al-Wahdah Teaching Hospital (TUWTH), between 2018 and 2019. Enterobius vermicularis infection was examined using the adhesive tape technique. Association between risk factors and enterobiasis were measured by prevalence ratio (PR). The overall prevalence of enterobiasis was found to be 29.4% (118/402). Risk factors that showed independent association with the infection were child’s care responsibility (PR = 1.90; 95% CI = 1.37–2.63; P = 0.001); irregular washing hands before meals (PR = 2.01; 95% CI = 1.32–3.05; P = 0.003); habit of nail biting or cutting by teeth (PR = 1.61; 95% CI = 1.18–2.21; P = 0.002); habit of putting toys or pen in mouth (PR = 1.58; 95% CI = 1.19–2.10; P = 0.002); frequent anal itching (PR = 1.46; 95% CI = 1.10–1.93; P = 0.016); using anthelmintic during the last six months (PR = 1.68; 95% CI = 1.20–2.36; P = 0.011); and parents have no knowledge on preventive measures (PR = 1.62; 95% CI = 1.04–2.53; P = 0.036). Prevalence of enterobiasis among Yemeni children in Dhamar governorate is high with higher infection rate among those aged 1–6 years. Health education and mass treatment are highly recommended among this poor population.
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Data supporting the conclusions of this article are included within the article. The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Afrakhteh N, Marhaba Z, Mahdavi SA, Garoosian S, Mirnezhad R, Vakili ME, Shahraj HA, Javadian B, Rezaei R, Moosazadeh M (2016) Prevalence of Enterobius vermicularis amongst kindergartens and preschool children in Mazandaran Province, North of Iran. J Parasit Dis 40(4):1332–1336. https://doi.org/10.1007/s12639-015-0683-z
Al-Mekhlafi AM, Abdul-Ghani R, Al-Eryani SM, Saif-Ali R, Mahdy MAK (2016) School-based prevalence of intestinal parasitic infections and associated risk factors in rural communities of Sana’a, Yemen. Acta Trop 163:135–141. https://doi.org/10.1016/j.actatropica.2016.08.009
Alyousefi NA, Mahdy MAK, Mahmud R, Lim YAL (2011) Factors associated with high prevalence of intestinal protozoan infections among patients in Sana’a City, Yemen. PLoS ONE 6(7):e22044. https://doi.org/10.1371/journal.pone.0022044
Anuar TS, Jalilah L, Norhayati M, Azlin MY, Fatmah MS, Al-Mekhlafi HM (2016) New insights of Enterobius vermicularis infection among preschool children in an urban area in Malaysia. Helminthologia 53(1):76–80
Bayoumy A, Ibrahim WLF, El Nour A, Basma M, Said AAA (2016) The parasitic profile among school children in El-wadi El-gadded governorate, Egypt. J Egypt Soc Parasitol 46(3):605–612
Burkhart CN, Burkhart CG (2005) Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). Int J Dermatol 44(10):837–840. https://doi.org/10.1111/j.1365-4632.2004.02332.x
Bustami F, Khraisha S (2010) Enterobius vermicularis infection in three refugee camps in Jordan. Jordan Medical Journal 44(4):432–436
Chai JY, Yang SK, Kim JW, Choi S-L, Song GY, Jung BK, Jung MJ, Cho J, Kim DG, Sohn WM, Jeoung HG, Cho S, Park JB, Hong S, Htoon TT, Tin HH (2015) High prevalence of Enterobius vermicularis infection among schoolchildren in three townships around Yangon, Myanmar. Korean J Parasitol 53(6):771. https://doi.org/10.3347/kjp.2015.53.6.771
Chang TK, Liao CW, Huang YC, Chang CC, Chou CM, Tsay HC, Huang A, Guu SF, Kao TC, Fan CK (2009) Prevalence of Enterobius vermicularis infection among preschool children in kindergartens of Taipei City, Taiwan in 2008. Korean J Parasitol 47(2):185. https://doi.org/10.3347/kjp.2009.47.2.185
Chu TB, Liao CW, Nara T, Huang YC, Chou CM, Liu YH, Fan CK (2012) Enterobius vermicularis infection is well controlled among preschool children in nurseries of Taipei City, Taiwan. Rev Soc Bras Med Trop 45:646–648. https://doi.org/10.1590/s0037-86822012000500020
Cook GC (1994) Enterobius Vermicularis Infection. Gut 35(9):1159. https://doi.org/10.1136/gut.35.9.1159
de la Luz Galván-Ramírez M, Madriz-Elisondo AL, Cynthia Guadalupe Temores R, Jorge de Jesús Romero R, de la O Carrasco, DA, López MAC (2019) Enteroparasitism and risk factors associated with clinical manifestations in children and adults of Jalisco State in Western Mexico. Osong Public Health Res Perspect 10(1):39. https://doi.org/10.24171/j.phrp.2019.10.1.08
Gunawardena NK, Chandrasena TGAN, de Silva NR (2013) Prevalence of enterobiasis among primary school children in Ragama. Sri Lanka Ceylon Med J 58(3):106–110. https://doi.org/10.4038/cmj.v58i3.5039
Gungoren B, Latipov R, Regallet G, Musabaev E (2007) Effect of hygiene promotion on the risk of reinfection rate of intestinal parasites in children in rural Uzbekistan. Trans R Soc Trop Med Hyg 101(6):564–569. https://doi.org/10.1016/j.trstmh.2007.02.011
Gyawali N, Amatya R, Nepal HP (2010) Intestinal parasitosis in school going children of Dharan municipality, Nepal. Trop Gastroenterol 30(3):145–147
Hong ST, Chai JY, Cho SY (1979) Efficacy of repeated chemotherapy in control of Enterobius vermicularis infection. Seoul J Med 20(3):163–168
Kang S, Jeon HK, Eom KS, Park J-K (2006) Egg positive rate of Enterobius vermicularis among preschool children in Cheongju, Chungcheongbuk-do, Korea. Korean J Parasitol 44(3):247. https://doi.org/10.3347/kjp.2006.44.3.247
Kim D-H, Son H-M, Kim JY, Cho MK, Park MK, Kang SY, Kim BY, Yu HS (2010) Parents’ knowledge about enterobiasis might be one of the most important risk factors for enterobiasis in children. Korean J Parasitol 48(2):121. https://doi.org/10.3347/kjp.2010.48.2.121
Kim D-H, Cho MK, Park MK, Kang SA, Kim BY, Park SK, Yu HS (2013) Environmental factors related to enterobiasis in a southeast region of Korea. Korean J Parasitol 51(1):139. https://doi.org/10.3347/kjp.2013.51.1.139
Lee S-E, Lee J-H, Ju J-W, Lee W-J, Cho S-H (2011) Prevalence of Enterobius vermicularis among preschool children in Gimhae-si, Gyeongsangnam-do, Korea. Korean J Parasitol 49(2):183. https://doi.org/10.3347/kjp.2011.49.2.183
Li H-M, Zhou C-H, Li Z-S, Deng Z-H, Ruan C-W, Zhang Q-M, Zhu T-J, Long-Qi Xu, Chen Y-D (2015) Risk factors for Enterobius vermicularis infection in children in Gaozhou, Guangdong, China. Infect Dis Poverty 4(1):1–8. https://doi.org/10.1186/s40249-015-0058-9
Lohiya G-S, Tan-Figueroa L, Crinella FM, Lohiya S (2000) Epidemiology and control of enterobiasis in a developmental center. West J Med 172(5):305. https://doi.org/10.1136/ewjm.172.5.305
Neghina R, Neghina AM, Marincu I, Iacobiciu I (2011) Intestinal nematode infections in Romania: an epidemiological study and brief review of literature. Vector-Borne Zoon Dis 11(8):1145–1149. https://doi.org/10.1089/vbz.2010.0178
Nithikathkul C, Changsap B, Wannapinyosheep S, Poister C, Boontan P (2001) The prevalence of Enterobius vermicularis among primary school students in Samut Prakan Province, Thailand. Southeast Asian J Trop Med Public Health 32:133–137
Olivares JL, Fernández R, Fleta J, Ruiz MY, Clavel A (2002) Vitamin B12 and folic acid in children with intestinal parasitic infection. J Am Coll Nutr 21(2):109–113. https://doi.org/10.1080/07315724.2002.10719202
Park J-H, Han E-T, Kim W-H, Shin E-H, Guk S-M, Kim J-L, Chai J-Y (2005) A survey of Enterobius vermicularis infection among children on western and southern coastal islands of the Republic of Korea. Korean J Parasitol 43(4):129. https://doi.org/10.3347/kjp.2005.43.4.129
Sah SP, Bhadani PP (2006) Enterobius vermicularis causing symptoms of appendicitis in Nepal. Trop Doct 36(3):160–162. https://doi.org/10.1258/004947506777978361
Suraweera OSA, Galgamuwa LS, Iddawela D, Wickramasinghe S (2015) Prevalence and associated factors of Enterobius vermicularis infection in children from a poor urban community in Sri Lanka: a cross-sectional study. Int J Res Med Sci 3(8):1994–1999
Tandan T, Pollard AJ, Money DM, Scheifele DW (2002) Pelvic inflammatory disease associated with Enterobius vermicularis. Arch Dis Child 86(6):439–440. https://doi.org/10.1136/adc.86.6.439
Totanes DG, Detras GGC, Kathryn MB, Jaucian MAA, Salazar ALT, Cauyan GA, dela Cruz-Papa DMA (2009) Comparative prevalence of Enterobius vermicularis between a coastal and Inland Barangay in Batangas and Cavite. Acta Manilana 57:9–18
Tsibouris P, Galeas T, Moussia M, Sotiropoulou M, Michopoulos S, Kralios N (2005) Two cases of eosinophilic gastroenteritis and malabsorption due to Enterobious vermicularis. Dig Dis Sci 50(12):2389–2392. https://doi.org/10.1007/s10620-005-3069-8
Wang S, Yao Z, Hou Y, Wang D, Zhang H, Ma J, Zhang L, Liu S (2016) Prevalence of Enterobius vermicularis among preschool children in 2003 and 2013 in Xinxiang city. Henan. https://doi.org/10.1051/parasite/2016030
Acknowledgements
The authors would like to thank the study participants and health staff at Thamar University Al-Wahdah Teaching Hospital (TUWTH) in Dhamar governorate, Yemen, for their cooperation during the study.
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AHA was involved in all phases of the study, including study design, data collection, data analysis and interpretation, the write-up of the manuscript, statistical analysis of data and the critical revision of the manuscript for publication; YAA, MAA and AH Amer were involved in the study design, specimen examination and revision of the manuscript; and MMA, FHA, RHA, ESA, SAA, TMA were involved in the collection of the data, specimen examination and write-up of the first draft of the manuscript. All authors read and approved the final manuscript.
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The protocol of this study was approved by the Thamar University Medical Ethics Committee (TUMRC) of Thamar University Faculty of Medicine and Health Sciences (TUFMHS), Dhamar (Reference Number: TUMRC-18001). All examinations were carried out with permission from the children’s parents. Oral informed consent was obtained before commencing the survey.
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Al-Adhroey, A.H., Al-Ansi, Y.A., Al-Kholani, M.A. et al. Enterobiasis among Yemeni children: a cross-sectional study. J Parasit Dis 46, 722–728 (2022). https://doi.org/10.1007/s12639-022-01487-1
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DOI: https://doi.org/10.1007/s12639-022-01487-1