Gastrointestinal helminthiasis among Nigerian farmers in Delta North communities

Abstract

Objective: To investigate the prevalence of gastrointestinal helminth infections among farmers of different age groups and the risk factors influencing disease transmission in different geographic settings with intermittent treatment in Delta North Agricultural Zone in Nigeria.
Methods: This cross-sectional study was carried out among all age groups in some farming communities in freshwater swamp forest and lowland rainforest of Delta North Agricultural Zone. Kato Katz method was used to detect gastrointestinal helminth infections in stool samples. Study participants totalled 20 698 including 11 215 (54.2%) males and 9 483 (45.8%) females. Additionally, diagnostic tests performance for Schistosoma mansoni using Kato Katz and PCR were compared.
Results: This study identified six parasites namely, Schistosoma mansoni, Ascaris lumbricoides, hookworm, Trichuris trichiura, Enterobius vermicularis and Strongyloides stercoralis, with a total prevalence of 21.6%. The freshwater swamp forest had a slightly higher prevalence (21.8%) with six parasite species than that of the lowland rainforest (21.0%) with five species, but the difference was not statistically significant (P > 0.05). Factors that influenced disease transmission include sex, age, behaviour, type of infection, culture and environment, with vulnerabilities higher among children and females (P < 0.05). Additional investigation comparing Kato Katz method and PCR using Schistosoma mansoni 121 bp primer on 120 samples showed prevalence of 0.0% for Kato Katz and 4.2% for PCR.
Conclusions: This study revealed persistent gastrointestinal helminth infections in areas where there is intermittent mass antihelminthic administration. This underscores the need for integrated control of gastrointestinal helminthiasis in farming communities.

Keywords

Gastrointestinal helminthiasis / Delta North Agricultural Zone / Farmers / Risk factors

Conflict of interest statement

The authors claim there is no conflict of interest.

Funding

This study receives no extramural funding.

Data availability statement

The data supporting the findings of this study are available from the corresponding author upon request.

Authors’ contributions

Enudi A was involved in the conception, design, data collection, analysis and interpretation, manuscript drafting, revision and approval. Nmorsi O was involved in the conception, design, data interpretation, revision and approval for publication. Egwunyenga A was involved in the conception, design, data interpretation, revision and approval for publication.

References

[1] Al Amin ASM, Wadhwa R. Helminthiasis [Online]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK560525/ [Accessed on 12 September 2023].

[2] Hotez PJ, Bundy DAP, Beegle K, Brooker S, Drake L, de Silva N, et al. Helminth Infections: Soil-transmitted Helminth Infections and Schistosomiasis. In: Jamison DT, Breman JG, Measham AR, et al., editors. Disease Control Priorities in Developing Countries. 2nd edition. Washington (DC): The International Bank for Reconstruction and Development / The World Bank; 2006. Chapter 24 [Online]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK11748/ [Accessed on 12 September 2023].

[3] Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: The great neglected tropical diseases. J Clin Invest 2008; 118(4): 1311-1121.

[4] Montresor A, Mupfasoni D, Mikhailov A, Mwinzi P, Lucianez A, Jamsheed M, et al. The global progress of soil-transmitted helminthiases control in 2020 and World Health Organization targets for 2030. PLoS Negl Trop Dis 2020; 14(8): e0008505.

[5] World Health Organization . Soil Transmitted Helminth Infections. [Online]. [18 January 2023]. Available from: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections#:~:text=More%20than%201.5%20billion%20people,Americas%2C%20China%20and%20East%20Asia. [Accessed on 5 October 2023].

[6] Delaluna JOC, Flores MJC, Belizario Jr VY, Janairo JIB, Derick Erl P, Sumalapao DEP. Soil-transmitted helminth egg contamination from soil of indigenous communities in selected barangays in Tigaon, Camarines Sur, Philippines. Asian Pac J Trop Med 2020; 13(9): 409-414.

[7] Yaro CA, Kogi E, Luka SA. Spatial distribution and modelling of soil transmitted helminthes infection in Nigeria. Res J Parasitol 2018; 13(2): 19-35.

[8] Hotez PJ, Kamath A. Neglected tropical diseases in sub-saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Negl Trop Dis 2009; 3(8): e412. doi: 10.1371/journal.pntd.0000412.

[9] Ganguly S, Barkataki S, Sanga P, Boopathi K, Kanagasabai K, Devika S, et al. Epidemiology of Soil-Transmitted Helminth Infections among Primary School Children in the States of Chhattisgarh, Telangana, and Tripura, India, 2015-2016. Am J Trop Med Hyg 2022; 107(1): 122-129.

[10] Mogaji HO, Johnson OO, Adigun AB, Adekunle ON, Bankole S, Dedeke GA, et al. Estimating the population at risk with soil transmitted helminthiasis and annual drug requirements for preventive chemotherapy in Ogun State, Nigeria. Sci Rep 2022; 12(1): 2027.

[11] World Health Organization . Ending the neglect to attain the Sustainable Development Goals: A road map for neglected tropical diseases 2021-2030 [Online]. Available from: https://www.who.int/publications/i/item/9789240010352. [Accessed on 17 December 2022].

[12] UNICEF, Federal Government of Nigeria . Evaluation of the UNICEF supported Federal Government of Nigeria Water, Sanitation and Hygiene Programme (2014-2017) [Online]. Available from: https://www.unicef.org/nigeria/media/2986/file/Evaluation%20Report%20on%20WASH%20Programme%202014%20-%202017.pdf. [Accessed on 2 December 2022].

[13] Hotez PJ, Asojo OA, Adesina AM. Nigeria: "Ground Zero" for the high prevalence neglected tropical diseases. PLoS Negl Trop Dis 2012; 6(7): e1600.

[14] Nigeria Federal Ministry of Health. National protocol for integrated epidemiological mapping and baseline survey of schistosomiasis and soil transmitted helminths (version 1.2) [Online]. Available from: https://health.gov.ng/doc/PROTOCOL-FOR-SCHISTO-STH-MAPPING-1.pdf. [Accessed on 28 November 2022].

[15] Federal Ministry of Health . Neglected Tropical Diseases Nigeria Multi-Year Master Plan 2015-2020 [Online]. Available from https://espen.afro.who.int/system/files/content/resources/NIGERIA_NTD_Master_Plan_2015_2020.pdf. [Accessed on 28 November 2022].

[16] Federal Ministry of Water Resources, Government of Nigeria, National Bureau of Statistics, UNICEF . Water, Sanitation and Hygiene: National Outcome Routine Mapping (WASH NORM) 2019: A report of findings [Online]. Available from: https://www.unicef.org/nigeria/media/3576/file/WASH%20NORM%20Report%202019.pdf. [Accessed on 29 November 2023].

[17] Federal Ministry of Water Resources, Government of Nigeria, National Bureau of Statistics, UNICEF . Water, Sanitation and Hygiene: National Outcome Routine Mapping (WASHNORM) 2021: A Report of Findings [Online]. Abuja. Federal Ministry of Water Resources; 2022. Available from: https://www.unicef.org/nigeria/media/5951/file/2021%20WASHNORM%20Report%20.pdf. [Accessed on 28 November 2023].

[18] Mogaji H, Dedeke G, Jaiyeola O, Adeniran A, Olabinke D, Oluwole A, et al. A preliminary survey of school-based water, sanitation, hygiene (WASH) resources and soil-transmitted helminthiasis in eight public schools in Odeda LGA, Ogun State, Nigeria. Parasitol Open 2017; 3: E16.

[19] Oyewole OE, Simon-Oke IA. Ecological risk factors of soil-transmitted helminths infections in Ifedore district, Southwest Nigeria. Bull Natl Res Cent 2022; 46: 13.

[20] Dejon-Agobé JC, Honkpehedji YJ, Zinsou JF, Edoa JR, Adégbitè BR, Mangaboula A, et al. Epidemiology of Schistosomiasis and Soil-Transmitted Helminth Coinfections among Schoolchildren Living in Lambaréné, Gabon. Am J Trop Med Hyg 2020; 103(1): 325-333.

[21] Hailu T, Amor A, Nibret E, Munshea A, Anegagrie M, Flores Chavez MD, et al. Evaluation of five diagnostic methods for Strongyloides stercoralis infection in Amhara National Regional State, northwest Ethiopia. BMC Infect Dis 2022; 22: 297.

[22] Gyang VP, Chuang TW, Liao CW, Lee YL, Akinwale OP, Orok A, et al. Intestinal parasitic infections: Current status and associated risk factors among school aged children in an archetypal African urban slum in Nigeria. J Microbiol Immunol Infect 2017; 52(1): 106-113.

[23] Lodh N, Shiff CJ, Mutengo MM, Mwansa JCL. Diagnosis of Schistosoma mansoni without the stool: Comparison of three diagnostic tests to detect Schistosoma mansoni infection from filtered urine in Zambia. Am J Trop Med Hyg 2013; 89(1): 46-50.

[24] Bartlett AW, Sousa-Figueiredo JC, van Goor RC, Monaghan P, Lancaster V, Mugizi R, et al. Burden and factors associated with schistosomiasis and soil-transmitted helminth infections among school-age children in Huambo, Uige and Zaire provinces, Angola. Infect Dis Poverty 2022; 11: 73. https://doi.org/10.1186/s40249-022-00975-z.

[25] Chisango TJ, Ndlovu B, Vengesai A, Nhidza AF, Sibanda EP, Zhou D, et al. Benefits of annual chemotherapeutic control of schistosomiasis on the development of protective immunity. BMC Infect Dis 2019; 19(1): 219.

[26] Kabatereine NB, Brooker S, Koukounari A, Kazibwe F, Tukahebwa EM, Fleming FM, et al. Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bull World Health Organ 2007; 85: 91-99.

[27] Balogun VS, Onokerhoraye AG. Climate change vulnerability mapping across ecological zones in Delta State, Niger Delta Region of Nigeria. Clim Serv 2022; 27: 100304.

[28] World Health Organization . Bench aids for the diagnosis of intestinal parasites. 2nd ed [Online]. Available from: https://www.who.int/publications/i/item/9789241515344. [Accessed on 14 December 2022].

[29] Cheesbrough M. District Laboratory Practice in Tropical Countries [Online]. Available from: https://medicallabtechno.weebly.com/uploads/7/5/1/5/7515789/monica-cheesbrough-district-laboratory-practice-in-tropical-countries-part-1.pdf. [Accessed 30 October 2022].

[30] Montresor A, Crompton DWT, Gyorkos TW, Savioli L. Helminth control in school-age children: A guide for managers of control programmes [Online]. Geneva: World Health Organization; 2002. Available from: https://iris.who.int/bitstream/handle/10665/44671/9789241548267_eng.pdf?sequence=1. [Accessed on 14 October 2023].

[31] Hamburger J, Turetski T, Kapeller I, Deresiewicz R. Highly repeated short DNA-sequences in the genome of Schistosoma mansoni recognized by a species-specific probe. Mol Biochem Parasitol 1991; 44: 73-80.

[32] Gbonhinbor J, Abah AE, Awi-Waadu G. Prevalence of intestinal parasitic infection and associated risk factors among primary school-aged children (5-15 years) in southern Nigeria. Int J Infect 2022; 9(3): e123721. doi: 10.5812/iji-123721.

[33] Idowu OA, Babalola AS, Olapegba T. Prevalence of soil-transmitted helminth infection among children under 2 years from urban and rural settings in Ogun state, Nigeria: implication for control strategy. Gaz Egypt Pediatr Assoc 2022; 70: 5.

[34] Woldegerima E, Bayih AG, Tegegne Y, Aemero M, Zeleke AJ. Prevalence and reinfection rates of Schistosoma mansoni and praziquantel efficacy against the parasite among primary school children in Sanja Town, Northwest Ethiopia. J Parasitol Res 2019; 2019: 3697216.

[35] Nmor JC, Onojafe JO, Omu BA. Anthropogenic indices of soil-transmitted helminthiasis among children in Delta State, Southern Nigeria. Iran J Public Health 2009; 38(3): 31-38.

[36] Bolaji OS, Awopetu OR, Akinleye AC, Bakare EO, Bolaji ES, Ukaga CN, et al. Detection by polymerase chain reaction of Schistosoma mansoni DNA in urine of school age children in parts of Osun State. J Chem Bio Phy Sci Sec B 2019; 9(4): 521-534.

[37] Labana RV, Romero VA, Guinto AM, Caril AN, Untalan KD, Reboa AJC, 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.

[38] Pezzani BC, Minvielle MC, de Luca MM, Cordoba MA, Apezteguia MC, Basualdo JA. Enterobius vermicularis infection among population of General Mansilla, Argentina. World J Gastroenterol 2004; 10(17): 2535-2539.

[39] Hailu T, Nibret E, Amor A, Munshea A. Strongyloidiasis in Africa: Systematic review and meta-analysis on prevalence, diagnostic methods, and study settings. BioMed Res International 2020; 2020: 2868564.

[40] Forrer A, Khieu V, Schär F, Vounatsou P, Chammartin F, Marti H, et al. Strongyloides stercoralis and hookworm co-infection: Spatial distribution and determinants in Preah Vihear Province, Cambodia. Parasit Vectors 2018; 11(1): 33.

[41] Mazigo HD, Uisso C, Kazyoba P, Nshala A, Mwingira UJ. Prevalence, infection intensity and geographical distribution of schistosomiasis among pre-school and school-aged children in villages surrounding Lake Nyasa, Tanzania. Sci Rep 2021; 11: 295.

[42] Mnkugwe RH, Minzi OS, Kinung'hi SM, Kamuhabwa AA, Aklillu E. Prevalence and correlates of intestinal schistosomiasis infection among school-aged children in North-Western Tanzania. PLoS One 2020; 15(2): e0228770.

[43] Spencer SA, Penney JM, Russell HJ, Howe AP, Linder C, Rakotomampianina ALD, et al. High burden of Schistosoma mansoni infection in school-aged children in Marolambo District, Madagascar. Parasites Vectors 2017; 10: 307.