Hemoglobin Level and Risk of Anemia in Soil-Transmitted Helminths Infections among Children: A Systematic Review and Meta-analysis
DOI:
https://doi.org/10.3889/oamjms.2022.8974Keywords:
Anemia, Children, Hemoglobin, Infection, Soil-transmitted helminthesAbstract
Introduction. Soil Transmitted Helminthiasis (STH) is a Neglected Tropical Disease with almost 25% world population infected. Children were vulnerable to infection with morbidities affecting growth. STH infection alters children nutritional status which potentially causing anemia. Meta-analysis relating STH infections to hemoglobin (Hb) level and risk of anemia in children is limited.
Aim. To compare hemoglobin levels and risk of anemia in children infected and uninfected with STH.
Methods. Meta-analysis conducted from journals obtained from Pubmed, ScienceDirect, WileyLibrary, Cochrane, EBSCO, Proquest, DOAJ, and GoogleScholar from 2011-2021. Full text cross sectional studies on children with relevant topic is included, while unclear, inaccessible, or post interventional studies were excluded. Articles were analyzed in Review Manager 5.4 in mean difference (MD) and odds ratio (OR) with Confidence Interval (CI) of 95%.
Result. Out of 25,683 articles in literature search, 29 were eligible for systematic review and meta-analysis. STH infection significantly decreases hemoglobin level (MD -0.2g/dL; p=0.02) and increases risk of anemia (OR 1.83; p<0.00001). Species analysis presented parallel result on Trichuris trichiura (MD -0.31g/dL; p=0.001 and OR 1.66; p=0.009), Hookworm (MD -0.56g/dL; p=0.02 and OR 3.3; p<0.00001), and multiple infection (MD -0.25g/dL; p=0.03 and OR 4.49; p=0.005). Ascaris lumbricoides didn’t show significance on hemoglobin level but comparable for risk of anemia (MD -0.16g/dL; p=0.17 and OR 1.57; p=0.001).
Discussion. All STH infections exhibits lower hemoglobin level and higher risk of anemia caused by lower nutrition absorption and occult bleeding in gastrointestinal tract. Hookworm and multiple infections has the highest risk of anemia. Proportion of anemia may vary in studies and influenced by sociodemographic characteristics, but higher proportions occur in STH infected.
Conclusion. Children infected with STH has lower hemoglobin level and in risk of anemia compared to uninfected children, hence further study is still needed to be conducted.
Keywords: Anemia, Children, Hemoglobin, Infection, Soil Transmitted Helminths
Downloads
Metrics
Plum Analytics Artifact Widget Block
References
Farrar J, Hotez PJ, Junghanss T, Kang G, Lalloo D, White NJ. Manson’s Tropical Diseases. 23rd ed. Philadelphia, PA: Elsevier Ltd.; 2014. p. 1337. https://doi.org/10.1016/b978-0-7020-5101-2.00094-7 DOI: https://doi.org/10.1016/B978-0-7020-5101-2.00094-7
Centers for Disease Control and Prevention. Parasites-soiltransmitted Helminths. CDC; 2020. Available from: https://www.cdc.gov/parasites/sth/index.html [Last accessed on 2021 Apr 03].
Gordon CA, Kurscheid J, Jones MK, Gray DJ, McManus DP. Soil-transmitted helminths in tropical Australia and Asia. Trop Med Infect Dis. 2017;2(4):56. https://doi.org/10.3390/tropicalmed2040056 DOI: https://doi.org/10.3390/tropicalmed2040056
World Health Organization. Soil-transmitted Helminthiases. Geneva: World Health Organization; 2020. Available from: https://www.who.int/health-topics/soil-transmittedhelminthiases#tab=tab_1 https://doi.org/10.1007/978-3-642-70841-1_5 [Last accessed on 2021 Apr 03]. DOI: https://doi.org/10.1007/978-3-642-70841-1_5
Al Amin AS, Wadhwa R. Helminthiasis. Treasure Island, FL: StatPearls; 2021. Available from: https://www.pubmed.ncbi.nlm.nih.gov/32809360 [Last accessed on 2021 Apr 03].
Suchdev PS, Davis SM, Bartoces M, Ruth LJ, Worrell CM, Kanyi H, et al. Soil-transmitted helminth infection and nutritional status among urban slum children in Kenya. Am J Trop Med Hyg. 2014;90(2):299-305. https://doi.org/10.4269/ajtmh.13-0560 PMid:24343884 DOI: https://doi.org/10.4269/ajtmh.13-0560
World Health Organization. Global Anemia Prevalence and Number of Individuals. Geneva: World Health Organization; 2008. Available from: https://www.who.int/vmnis/anaemia/prevalence/summary/anaemia_data_status_t2/en [Last accessed on 2021 Oct 25].
Kassebaum NJ, Fleming TD, Flaxman A, Phillips DE, Steiner C, Barber RM, et al. The global burden of anemia. Hematol Oncol Clin North Am. 2016;30(2):247-308. http://doi.org/10.1016/j.hoc.2015.11.002 PMid:27040955 DOI: https://doi.org/10.1016/j.hoc.2015.11.002
Abanyie FA, McCracken C, Kirwan P, Molloy SF, Asaolu SO, Holland CV, et al. Ascaris co-infection does not alter malariainduced anaemia in a cohort of Nigerian preschool children. Malar J. 2013;12(1):1-9. https://doi.org/10.1186/1475-2875-12-1 PMid:23282136 DOI: https://doi.org/10.1186/1475-2875-12-1
Cho FN, Ngala HN, Bongazi RT, Kinsam RS, Tata BT, Aji D, et al. Effects of soil-transmitted helminths and intestinal protozoan infections on haemoglobin levels among schoolaged children in belo and Bui, North West Cameroon: A crosssectional study. J Parasitol Res. 2021;2021:8873555. https://doi.org/10.1155/2021/8873555 DOI: https://doi.org/10.1155/2021/8873555
De Gier B, Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, Van De Bor M, et al. Species-specific associations between soil-transmitted helminths and micronutrients in Vietnamese schoolchildren. Am J Trop Med Hyg. 2016;95(1):77-82. https://doi.org/10.4269/ajtmh.15-0533 PMid:27246448 DOI: https://doi.org/10.4269/ajtmh.15-0533
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):1-17. https://doi.org/10.1371/journal.pntd.0003877 PMid:26110518 DOI: https://doi.org/10.1371/journal.pntd.0003877
Matangila JR, Doua JY, Linsuke S, Madinga J, Inocêncio Da Luz R, Van Geertruyden JP, et al. Malaria, schistosomiasis and soil transmitted helminth burden and their correlation with anemia in children attending primary schools in kinshasa, democratic republic of congo. PLoS One. 2014;9(11):e110789. https://doi.org/10.1371/journal.pone.0110789 PMid:25372029 DOI: https://doi.org/10.1371/journal.pone.0110789
Müller I, Yap P, Steinmann P, Damons BP, Schindler C, Seelig H, et al. Intestinal parasites, growth and physical fitness of schoolchildren in poor neighbourhoods of Port Elizabeth, South Africa: A cross-sectional survey. Parasites Vectors. 2016;9(1):1-14. http://doi.org/10.1186/s13071-016-1761-5 PMid:27595566 DOI: https://doi.org/10.1186/s13071-016-1761-5
Muñoz-Antoli C, Pérez P, Pavón A, Toledo R, Esteban JG. Soiltransmitted helminth infections and anemia in schoolchildren from Corn Island archipelago (RAAS, Nicaragua). Am J Trop Med Hyg. 2018;99(6):1591-7. https://doi.org/10.4269/ajtmh.18-0195 PMid:30298802 DOI: https://doi.org/10.4269/ajtmh.18-0195
Sanchez AL, Gabrie JA, Usuanlele MT, Rueda MM, Canales M, Gyorkos TW. Soil-transmitted helminth infections and nutritional status in school-age children from rural communities in honduras. PLoS Negl Trop Dis. 2013;7(8):e2378. https://doi.org/10.1371/journal.pntd.0002378 PMid:23951385 DOI: https://doi.org/10.1371/journal.pntd.0002378
Staudacher O, Heimer J, Steiner F, Kayonga Y, Havugimana JM, Ignatius R, et al. Soil-transmitted helminths in southern highland Rwanda: Associated factors and effectiveness of school-based preventive chemotherapy. Trop Med Int Health. 2014;19(7):812-24. https://doi.org/10.1111/tmi.12321 PMid:24750543 DOI: https://doi.org/10.1111/tmi.12321
Sumbele IU, Nkain AJ, Ning TR, Anchang-Kimbi JK, Kimbi HK. Influence of malaria, soil-transmitted helminths and malnutrition on haemoglobin level among school-aged children in Muyuka, Southwest Cameroon: A cross-sectional study on outcomes. PLoS One. 2020;15(3):1-19. https://doi.org/10.1371/journal.pone.0230882 PMid:32226023 DOI: https://doi.org/10.1371/journal.pone.0230882
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. https://doi.org/10.4038/sljid.v8i2.8226 DOI: https://doi.org/10.4038/sljid.v8i2.8226
Verhagen LM, Incani RN, Franco CR, Ugarte A, Cadenas Y, Sierra Ruiz CI, et al. High malnutrition rate in venezuelan yanomami compared to warao amerindians and creoles: Significant associations WITH intestinal parasites and anemia. PLoS One. 2013;8(10):1-13. https://doi.org/10.1371/journal.pone.0077581 PMid:24143243 DOI: https://doi.org/10.1371/journal.pone.0077581
Wijaya W, Pasaribu AP, Yanni GN, Suteno E, Husin N, Pasaribu S. Correlation between soil-transmitted helminths and anemia incidence in primary school children in talawi, batubara regency. Open Access Maced J Med Sci. 2021;9(T3):325-9. https://doi.org/10.3889/oamjms.2021.6357 DOI: https://doi.org/10.3889/oamjms.2021.6357
Alaribi FI, Unyah NZ, Misni N, Masri SN, Osman M. The prevalence of soil-transmitted helminths infection and its association with anaemia among refugee school children in the Klang Valley, Malaysia. Malaysian J Med Heal Sci. 2020;16(4):46-53.
Alelign T, Degarege A, Erko B. Prevalence and factors associated with undernutrition and anaemia among school children in Durbete Town, northwest Ethiopia. Arch Public Health. 2015;73(1):34. https://doi.org/10.1186/s13690-015-0084-x PMid:26261719 DOI: https://doi.org/10.1186/s13690-015-0084-x
Hailu Amare H, Lindtjørn B. Helminth infections among rural schoolchildren in Southern Ethiopia: A cross-sectional multilevel and zero-inflated regression model. PLoS Negl Trop Dis. 2020;14(12):1-24. https://doi.org/10.1371/journal.pntd.0008002 DOI: https://doi.org/10.1371/journal.pntd.0008002
Belizario VY, Totañes FI, de Leon WU, Lumampao YF, Ciro RN. Soil-transmitted helminth and other intestinal parasitic infections among school children in indigenous people communities in Davao del Norte, Philippines. Acta Trop. 2011;120(1):12-8. https://doi.org/10.1016/j.actatropica.2011.02.010 PMid:21396344 DOI: https://doi.org/10.1016/j.actatropica.2011.02.010
Darlan DM, Ananda FR, Sari MI, Arrasyid NK, Sari DI. Correlation between iron deficiency anemia and intestinal parasitic infection in school-age children in Medan. IOP Conf Ser Earth Environ. 2018;125(1):1-7. https://doi.org/10.1088/1755-1315/125/1/012059 DOI: https://doi.org/10.1088/1755-1315/125/1/012059
Djuardi Y, Lazarus G, Stefanie D, Fahmida U, Ariawan I, Supali T. Soil-transmitted helminth infection, anemia, and malnutrition among preschool-age children in nangapanda subdistrict, indonesia. PLoS Negl Trop Dis. 2021;15(6):1-17. https://doi.org/10.1371/journal.pntd.0009506 PMid:34138863 DOI: https://doi.org/10.1371/journal.pntd.0009506
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):1-14. https://doi.org/10.1371/journal.pone.0190151 PMid:29284032 DOI: https://doi.org/10.1371/journal.pone.0190151
Grimes JE, Tadesse G, Gardiner IA, Yard E, Wuletaw Y, Templeton MR, et al. Sanitation, hookworm, anemia, stunting, and wasting in primary school children in southern Ethiopia: Baseline results from a study in 30 schools. PLoS Negl Trop Dis. 2017;11(10):1-18. https://doi.org/10.1371/journal.pntd.0005948 PMid:28991894 DOI: https://doi.org/10.1371/journal.pntd.0005948
Kebede SW, Beyene DA, Meshesha AG, Sinishaw MA. Two thirds of hookworm infected children were anemic at the outpatient department in Jimma Health Center, Jimma, Southwest Ethiopia. Asian Pac J Trop Dis. 2016;6(9):691-4. https://doi.org/10.1016/s2222-1808(16)61111-8 DOI: https://doi.org/10.1016/S2222-1808(16)61111-8
Ketema H, Biruksew A, Mekonnen Z. Prevalence of Necator americanus infection and risk factors among school-age children in Mirab Abaya District, South Ethiopia. Asian Pacific J Trop Dis. 2015;5(5):363-8. https://doi.org/10.1016/s2222-1808(14)60798-2 DOI: https://doi.org/10.1016/S2222-1808(14)60798-2
Molla E, Mamo H. Soil-transmitted helminth infections, anemia and undernutrition among schoolchildren in Yirgacheffee, South Ethiopia. BMC Res Notes. 2018;11(1):1-7. https://doi.org/10.1186/s13104-018-3679-9 PMid:30103797 DOI: https://doi.org/10.1186/s13104-018-3679-9
Oliveira D, Ferreira FS, Atouguia J, Fortes F, Guerra A, Centeno-Lima S. Infection by intestinal parasites, stunting and anemia in school-aged children from Southern Angola. PLoS One. 2015;10(9):1-10. https://doi.org/10.1371/journal.pone.0137327 PMid:26371758 DOI: https://doi.org/10.1371/journal.pone.0137327
Osazuwa F, Ayo OM, Imade P. A significant association between intestinal helminth infection and anaemia burden in children in rural communities of Edo state, Nigeria. N Am J Med Sci. 2011;3(1):30-4. PMid:22540060 DOI: https://doi.org/10.4297/najms.2011.330
Subahar R, Susanto L, Astuty H, Winita R, Sari IP. Intestinal parasitic infections and hemoglobin levels among schoolchildren participating in a deworming program in Jakarta, Indonesia: A cross-sectional study. Open Access Maced J Med Sci. 2020;8(E):589-94. https://doi.org/10.3889/oamjms.2020.5153 DOI: https://doi.org/10.3889/oamjms.2020.5153
Sumbele IU, Nkemnji GB, Kimbi HK. Soil-transmitted helminths and plasmodium falciparum malaria among individuals living in different agroecosystems in two rural communities in the mount Cameroon area: A cross-sectional study. Infect Dis Poverty. 2017;6(1):1-16. https://doi.org/10.1186/s40249-017-0266-6 PMid:28302147 DOI: https://doi.org/10.1186/s40249-017-0266-6
Tandoh MA, Mills-Robertson FC, Wilson MD, Anderson AK. Nutritional and cognitive deficits of school-age children: A study in helminth-endemic fishing and farming communities in Ghana. Nutr Food Sci. 2020;50(3):443-62. https://doi.org/10.1108/nfs-01-2019-0035 DOI: https://doi.org/10.1108/NFS-01-2019-0035
Salam N, Fareed M. Soil transmitted helminth infections and its association with haemoglobin levels in India: A meta-analysis. J Clin Diagnostic Res. 2019;13(6):12. https://doi.org/10.7860/jcdr/2019/40681.12950 DOI: https://doi.org/10.7860/JCDR/2019/40681.12950
Naing C, Whittaker MA, Nyunt-Wai V, Reid SA, Wong SF, Mak JW, et al. Malaria and soil-transmitted intestinal helminth co-infection and its effect on anemia: A meta-analysis. Trans R Soc Trop Med Hyg. 2013;107(11):672-83. https://doi.org/10.1093/trstmh/trt086 PMid:24123127 DOI: https://doi.org/10.1093/trstmh/trt086
Righetti AA, Koua AY, Adiossan LG, Glinz D, Hurrell RF, N’Goran EK, et al. Etiology of anemia among infants, schoolaged children, and young non-pregnant women in different settings of South-Central Côte d’Ivoire. Am J Trop Med Hyg. 2012;87(3):425-34. https://doi.org/10.4269/ajtmh.2012.11-0788 PMid:22848097 DOI: https://doi.org/10.4269/ajtmh.2012.11-0788
Ahmed A, Al-Mekhlafi HM, Al-Adhroey AH, Ithoi I, Abdulsalam AM, Surin J. The nutritional impacts of soil-transmitted helminths infections among Orang Asli schoolchildren in rural Malaysia. Parasites Vectors. 2012;5(1):1-9. https://doi.org/10.1186/1756-3305-5-119 PMid:22704549 DOI: https://doi.org/10.1186/1756-3305-5-119
Sungkar S, Tambunan FB, Gozali MN, Kusumowidagdo G, Wahdini S. The effect of albendazole toward anemia in children with soil-transmitted helminths infection in a remote and endemic area. Med J Indones. 2018;27(4):293-8. https://doi.org/10.13181/mji.v27i4.2857 DOI: https://doi.org/10.13181/mji.v27i4.2857
Ness TE, Agrawal V, Bedard K, Ouellette L, Erickson TA, Hotez P, et al. Maternal hookworm infection and its effects on maternal health: A systematic review and meta-analysis. Am J Trop Med Hyg. 2020;103(5):1958-68. https://doi.org/10.4269/ajtmh.20-0503 PMid:32840198 DOI: https://doi.org/10.4269/ajtmh.20-0503
Ngui R, Lim YA, Kin LC, Chuen CS, Jaffar S. Association between anaemia, iron deficiency anaemia, neglected parasitic infections and socioeconomic factors in rural children of West Malaysia. PLoS Negl Trop Dis. 2012;6(3):1-9. https://doi.org/10.1371/journal.pntd.0001550 PMid:22413027 DOI: https://doi.org/10.1371/journal.pntd.0001550
Downloads
Published
How to Cite
Issue
Section
Categories
License
Copyright (c) 2022 Ahmad Razi Maulana Alnaz, Dewi Masyithah Darlan, Yunilda Andriyani, Rodiah Rahmawaty Lubis (Author)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
http://creativecommons.org/licenses/by-nc/4.0
