UMYU Journal of Microbiology Research

E-ISSN: 2814 – 1822; P-ISSN: 2616 – 0668

REVIEW ARTICLE

Soil-transmitted Helminth (STH) Infections in Northern Nigeria between 2000-2022: A Review

Adamu Rabiu^1,2, Nor Azwady Abd Aziz¹, Muskhazli Mustafa¹ & Shamarina Shohaimi¹

¹Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia

²Department of Biology, School of Secondary Education (Sciences), Federal College of Education (Technical) Bichi, Kano, 703101 Kano State, Nigeria

Corresponding Author: rabiuadamu15@gmail.com

Abstract

Soil-transmitted helminth (STH) infections, caused by parasitic nematodes, are significant public health concern in many parts of the world, including Nigeria. This review aims to comprehensively analyze the available studies and research trends on STH infections among children aged 0 – 17 years in northern Nigeria. The review focuses studies on the prevalence and risk factors related to STH infections from year 2000 – 2022 in this specific region and emphasizes the urgent need for effective control measure to mitigate the burden of these infections. The population involved 25 studies (92.6%) on School-aged Children (SAC) and 2 studies (7.4%) on Pre-school age Children (PSAC). A total of 8 514 children examined, 4 384 (51.5%) males and 4 130 (48.5%) females. Children from rural areas were 5 165 (60.7%) and 3 349 (39.3%) children from urban areas. Sample size ranges from 100 – 620, 22 (74.1%) studies employed Formol-ether concentration as stool examination technique, 4 (14.8%) and 3 (11.1%) used Kato-Katz and Direct smear methods respectively. The overall pool prevalence estimates (PPE) for STH infections were 3 160 (37.1%, 95% CI: 36.5–37.7). PPE for males 1 880 (59.5%, 95% CI: 58.6–60.1) was higher than for females 1 280 (40.5%, 95% CI: 54.2–55.3). Children from rural areas had the highest PPE 1 955 (37.9%) OR 1.26 (95% CI: 0.32–3.73) p=0.02, while children from urban areas had 3 160 (35.9%) OR 1.15 (95% CI: 0.62–5.02) p=0.01. There was no significant association between STH infections and community settings among SAC and PSAC. The most common PPEs by species identified was Ascaris lumbricoides 1 022 (32.3%, 95% CI: 31.7–32.9), hookworm 931 (29.5%, 95% CI: 28.9 – 30.1) and the least; Trichuris trichjura 356 (11.3%, 95% CI: 10.7 – 11.9). Children between 10 – 15 years had highest prevalence (48.6%), and 0 – 9 years had the least prevalence (23.5%) by age groups. Four common risk factors identified, walking barefooted 6 (22.2%) OR 1.16 (95% CI: 1.53 - 6.42) p-0.44, drinking untreated water 12 (44.4%) OR 1.66 (95% CI: 1.30 - 19.49) p=0.53, open field or bush defecation 8 (29.6) OR 3.41 (95% CI: 1.94 - 9.32) p=0.72 and eating unwashed fruits or vegetable 1 (3.7) OR 2.01 (95% CI: 1.32 - 4.51) p=0.54. The research underscores the need for enhanced surveillance, improved sanitation, and comprehensive sustainable interventions to reduce the prevalence and morbidity associated with STH infections in northern Nigeria.

Keywords: Soil-transmitted Helminthes, prevalence, risk factors, children, northern Nigeria.

INTRODUCTION

Soil-transmitted helminth infections, including those caused by roundworms (Ascaris lumbricoides), whipworms (Trichuris trichiura), and hookworms (Ancylostoma duodenale and Necator americanus), affect millions of people worldwide (World Health Organization, 2022), particularly in low-resource settings (Hailegebriel et al., 2020) Nigeria, the most populous country in Africa, with its diverse geographical and socioeconomic characteristics, is heavily burdened by these infections (Yahaya et al., 2015; Abdulhadi, 2017; Dahal et al., 2019) Soil-transmitted helminths (STH) are spread principally through contact with feces of infected people and penetration of hookworm larvae which thrive in warm and moist soil of most tropical and subtropical countries (Bethony et al., 2006). These helminthes are collectively referred to as geohelminths and usually co-infect their host (Ojha et al., 2014). These geohelminthes are identified using their respective ova (Bhumbla, 2018) The developmental stages of the nematodes causing STH are partly in the soil and in vertebrate host(s) (Loukouri et al., 2019) Soil-transmitted helminth may impact on the mental health of children as well as bring about malnutrition leading to growth retardation (Karagiannis-Voules et al., 2015) However, there is a paucity of comprehensive literature reviews focusing specifically about STH infections in the northern region of the country. This review aims to provide an in-depth analysis of the prevalence and risk factors associated with STH infections in northern Nigeria to bridge knowledge gap by systematically examining relevant studies conducted in this area.

METHODOLOGY

Search Strategy

A systematic literature search using a predefined search strategy was conducted in 11 electronic databases (Annual Review, Cambridge Core, CABI, Elsevier Scopus, Nature, Oxford Academic, PubMed, Google Scholar, Science Direct, Royal Society and World Scientific). The following were used as keywords in the search: (“Soil-transmitted helminths” OR “Ascaris lumbricoides” OR “Trichuris trichiura” OR “Ancylostoma duodenale” OR “Necator americanus” OR “Roundworm” OR “Whipworm” OR “Hookworm”), AND (“prevalence”), OR (“risk factors”) AND (“children”) AND (“northern Nigeria”). Studies published in English from January 2000 to September 2022 were considered for inclusion. The systematic review and selection of relevant literature were conducted according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) guidelines. Prevalence data from the surveyed States categorized under study area locations were analyzed. PICO elements were considered as the search strategies; thus, Population (northern Nigeria), Exposure (Soil-transmitted helminthiasis), Comparison (urban and rural area), and Outcome (prevalence, risk factors, and authors recommendations). Original laboratory-based studies and field studies with clearly stated location, sample sizes (n ≥ 100), and number of positive samples were considered for inclusion. Searches were restricted to northern regions; the north-central, north-east and north-west states of Nigeria. This review focused on prevalence, population and outcome because all screened articles were observational studies.

Study Area

Nigeria is situated in the West African region and lies between longitudes 3 degrees and 14 degrees and latitudes 4 degrees and 14 degrees. It has a land mass of 923,768 sq.km with a population of over 200 million people which covers a surface area of 923 768 km² in the sub-Saharan African region (Adeleye et al., 2023) It has two distinct seasons; the rainy season which runs from March to November in the southern region and May to October in the northern region as well as the dry season which runs from December to February in the south and November to April in the North (Adewole & Serifat, 2015) Nigeria is divided into six geopolitical zones (Figure 1), each of which has multiple states (Chinweuba et al., 2014; Monyei et al., 2023) These are the Northcentral (Plateau, Niger, Kwara, Nasarawa, Abuja, Kogi, Benue States), Northeast (Taraba, Bauchi, Gombe, Adamawa, Borno, Yobe States), Northwest (Kaduna, Zamfara, Katsina, Kano, Sokoto, Jigawa, Kebbi States), Southeast (Abia, Imo, Anambra, Ebonyi, Enugu State), South-South (Edo, Akwa Ibom, Rivers, Bayelsa, Cross River, Delta States) and Southwest (Oyo, Osun, Ogun, Lagos, Ekiti, Ondo States) geopolitical zones.

Inclusion Criteria and Exclusion Criteria

Studies screened for relevance based on inclusion requirement stated and duplicates were removed. Detailed abstract reviewed for eligibility and presence of the outcome of interest on the following conditions:

Studies were included if they:

1. Focused on soil-transmitted helminth infections in northern Nigeria.

2. Published in English.

3. Assessed the prevalence, population, gender, age group and risk factors of STH infections.

4. Sample size and number of positive cases clearly stated.

5. Presented original research findings.

6. Reported STH infections in Nigerian children.

7. Published in national and international reputable peer-reviewed journal.

Studies were excluded if they:

1. Were conducted outside the geographical scope of northern Nigeria

2. Primarily targeted non-soil-transmitted helminth infections.

3. Reported STH infections in other animals.

4. Were systematic reviews, or meta-analyses.

5. Were case reports, letters, editorials, or conference abstracts.

Figure 1: Nigeria geopolitical zones; South-West (SW), South-East (SE), North-West (NW), North-East (NE), North-Central (NC) and South-South (SS).

Data Extraction and Synthesis

Data extraction and synthesis were conducted to analyze the location, prevalence rates, methodology, and risk factors pertaining to STH infections in northern Nigeria. Selected articles were organized by study characteristics (author, year, methodology), study population, and sample sizes. The extracted data were synthesized thematically and presented using charts and tables. The prevalence of each STH in the study area was determined by dividing the total number of study participants by the number of STH-positive subjects. A 95 percent confidence interval (CI) was employed for assessing the overall prevalence. Mean differences are significant at 95% C.I., (p < 0.05) alpha value.

RESULTS AND DISCUSSIONS

Study Selection

The refined search yielded a total of 1313 studies that reported STH infection among children in northern Nigeria available in selected online databases (Table 1), and 15 studies retrieved manually. Mendeley reference manager version 2.103.0 was used for screening the downloaded articles.

Figure 2: Flow diagram of screened document for inclusion in the review on STH in northern Nigeria.

Table 1: Databases Search Result

A total of 937 articles were removed due to duplications, 36 articles were excluded for referring to other animals, 58 systematic reviews or meta-analyses studies were excluded, and 45 articles were excluded based on abstract, 8 articles with unstated numbers of positive samples and sample sizes (Figure 2). Twenty-seven articles were selected for this literature review.

Pooled Prevalence Distribution of STH infections in northern Nigeria

Table 2 summarizes the population and study area of STH infections reported in different regions of northern Nigeria. Twenty-five (92.6%) studies were reported among school-aged children, while 2 (7.4%) of the studies were reported among pre-school-aged children. The prevalence of STH infections among eligible studies ranged between 6.0 and 96.1%. Sixteen (59.3%) studies were conducted in rural areas, and 11 (40.7) were carried out in urban areas.

Pooled prevalence estimates (PPE) for STH infections are presented in Table 3. The included studies reported prevalence rates ranging from 2.7% and 76.1%, with significant regional variations. The sample sizes ranged between 100 – 620, with 5,165 (60-7%) children from rural areas and 3,349 (39.3%) children from urban areas. Formol-ether concentration was a commonly used technique for stool examination by 20 (74.1%) studies, 4 (14.8%) studies used Kato-Katz, and 3 (11.1%) applied Direct smear method. A total of 3,160 of the 8,514 northern Nigerian children examined during the period under review were infected with one or more species of STHs, yielding an overall PPE of 37.1% (95% CI: 32.4–39.5).

Ascaris lumbricoides had the highest PPE of 1,022; 32.3% (95% CI: 31.5–33.9) while Hookworms and Trichuris trichiura recorded PPEs of 931; 29.6% (95% CI: 29.0–30.2) and 356; 11.3% (95% CI: 10.7–11.9) respectively (Table 4). Out of 9.384 (51.5%) males and 4,130 (48.5) females examined (Table 5), males had the highest infection rate PPE of 1,880; 59.5% (95% CI: 58.1- 60.1) and females had 1,280; 20.5% (95% CI: 19.1–21.1). The studies used varieties of age intervals; consistent age-group intervals were 3, 4 and 5 (75.8%). Age highest PPE of 88.0% was recorded between 6 – 17 years, and least PPE of 0.0% was recorded in older children between the ages 16 -20 years. (Table 6).

Risk factors of STH infections in Northern Nigeria

Table 7 presents the identified risk factors associated with STH infections in northern Nigeria. Common risk factors include, Drinking untreated water 12 (44.4%); OR 1.66 (95% CI: 1.30 - 19.49) p=0.53, Open field or Bush defecation 8 (29.6%); OR 3.41 (95% CI: 1.94 - 9.32) p=0.72.

Table 2: Study Area and Population of STH infections in northern Nigeria

Walking barefooted 6(22.2%); OR 1.16 (95% CI: 1.53 - 6.42) p=0.44 and eating unwashed fruits and/or vegetables 1 (3.7%); OR 2.01 (95% CI: 1.32 - 4.51) p=0.54. School Health Services recommended in all primary and Secondary schools 7 (25.9), Regular deworming and provision of portable drinking water is needed 6 (22.2), Sanitation and improved personal hygiene, regular health education and portable drinking water and implementation of sustainable intervention measures were the common recommendations made by the authors.

The findings of this systematic review highlight the significant burden of STH infections in northern Nigeria (Yahaya et al., 2015; Taiwo et al., 2019; Funso-Aina et al., 2020) The prevalence rates varied across different regions, emphasizing the need for region-specific interventions (Attahiru Adamu & Bashir Abdulkadir, 2017; Yusuf et al., 2018)Twenty-five (92.6%) studies were reported among SAC while 2 (7.4%) of the studies were reported among PSAC. The prevalence of STH infections among eligible studies ranged between 6.0 and 96.1%. The finding is, however, within the range of 52.4–65.8% reported from other sub-Saharan African countries (Karagiannis-Voules et al., 2015). Study 2016 revealed a 36.4% decline in the prevalence of STH infections within a period of twenty-four years in India (Sardar et al., 2016a) STH studies in Nigeria have been focused mostly on children (preschool and school-age) (69%) than adults (31%), and mostly in rural (68.9%) than urban areas (31.1%) (Taiwo et al., 2019) Kumar et al. 2000 review 18 articles in Malaysia, the overall prevalence of STH was in range 7.56 to 78.27% (Nisha et al., 2020) Oluwatobiloba in Nigeria review STH articles between 2006 – 2015 revealed that prevalence of intestinal helminth in the country has not declined since the 1970s (Funso-Aina et al., 2020).

Table 3: Pooled Prevalence Distribution of STH Infections in Northern Nigeria

More than half of the studies were conducted in rural community settings 16 (59.3%) and 11 (40.7) were carried out in urban areas. The sample sizes ranged between 100 – 620, with an overall total of 5,165 (60-7%) children from rural areas and 3,349 (39.3%) children from urban areas. This is consistent with other studies (Ohiolei et al., 2017; Hailegebriel et al., 2020;) The prevalence of STH was higher in the rural population compared to the urban (Bhumbla, 2018; Santosh K. A., 2012) population, which is most likely on account of behaviors found in rural children such as defecation in open fields (Samuel, 2015), poor hygiene practices, such as having untrimmed fingernails, dirt under the nails, and lack of footwear (Yahaya et al., 2015; Taiwo et al., 2019) Several studies in Ethiopia also revealed that intestinal parasite infections are widely distributed with higher prevalence rates in rural community (Fauziah et al., 2022).(World Health Organization, 2021)

Table 4: Pooled Prevalence of STH Parasites Distribution in northern Nigeria

Parasitic infections were determined mainly using Formol-ether concentration technique 20 (74.1%) and Kato-Katz 4 (14.8%). FECT was more successful in detecting light infections (World Health Organization, 2022) and has the advantages of detecting other intestinal parasites and preservation of fecal samples (Santosh, 2012; Bhumbla, 2018); it has become the method of choice, formal ether concentration method is considered to be better compared to the others (Allen & Ridley, 1970; Fitriani et al., 2018; Suwansaksri et al., 2002).

Table 5: Gender-specific Pooled Prevalence of STH Infections in Northern Nigeria

In this study, 3,160 of the 8,514 northern Nigerian children examined during the period under review were infected with one or more species of STHs, yielding an overall PPE of 37.1% (95% CI: 32.4–39.5). The overall pooled prevalence estimate observed in the present study is higher than the 24.1% (Hailegebriel et al., 2020) and 25.4% (Sardar et al., 2016b) reported in Ethiopia and India, respectively. The northern zones have the worst spread and highest average prevalence for all helminthiases (Funso-Aina et al., 2020). Karshima in Nigeria reported a higher PPE of 54.8%, a total of 46 338 children (Male = 23 374 and Female = 22 964) in the 70 eligible studies (Karshima, 2018). In 2022, Nisa Fauziah et al. studied 17 articles in review related to STH infection in stunted children; PPE ranged from 12.5% to 56.5% (Fauziah et al., 2022).

Ascaris lumbricoides had the highest PPE of 1,022; (32.3%, 95% CI: 31.5–33.9) while Hookworms and Trichuris trichiura recorded PPEs of 931; (29.6%, 95% CI: 29.0–30.2) and 356; (11.3%, 95% CI: 10.7–11.9) respectively. This result agrees with previous findings of a greater Ascaris lumbricoides risk in peri-urban rather than rural regions and two hookworm species Ancylostoma duodenale and Necator americanus are endemic in South America (Chammartin et al., 2013), but their distribution, infection prevalence, and regional burden are poorly understood. The prevalence data in Nigeria showed a reduction in Ascaris lumbricoides and Trichuris trichiura infections, while infections with hookworm showed an irregular pattern with no significant differences (Imam et al., 2019). The prevalence of Ascaris lumbricoides, Ancylostoma duodenale and Trichuris trichiura in India was in the range between 0.4 to 71.87%, 0.14 to 42%, and 0.3 to 29.57%, respectively (Jayaram et al., 2021) This relative difference in prevalence of the three STHs is observed similarly across all regions of all countries and has been persistent even before independent review studies. The current study also suggests that Ascaris lumbricoides are the highest in northern Nigeria; this can be attributed to the ownership of domestic animals and improper hand-washing practices, especially after defecating. In contrast, another study showed a decreasing trend in prevalence for A. lumbricoides, and T. trichiura (6·6%, and 4·4%) among school-aged children from 2000 onwards in sub-Saharan Africa (Sartorius et al., 2020).

Table 6: High and Least Pooled Prevalence by Age of STH Infections in Northern Nigeria

Ascaris lumbricoides had the highest PPE of 1,022 (32.3%, 95% CI: 31.5–33.9), while Hookworms and Trichuris trichiura recorded PPEs of 931; (29.6%, 95% CI: 29.0–30.2) and 356; (11.3%, 95% CI: 10.7–11.9) respectively (Figure 3). This result agrees with previous findings of a greater Ascaris lumbricoides risk in peri-urban rather than rural regions and two hookworm species Ancylostoma duodenale and Necator americanus are endemic in South America (Chammartin et al., 2013), but their distribution, infection prevalence, and regional burden are poorly understood.

Figure 3: Pooled Prevalence Estimates (PPE)

Table 7: Risk factors of STH Infections in northern Nigeria

The prevalence data in Nigeria showed a reduction in Ascaris lumbricoides and Trichuris trichiura infections, while infections with hookworm showed an irregular pattern with no significant differences (Imam et al., 2019). The prevalence of Ascaris lumbricoides, Ancylostoma duodenale and Trichuris trichiura in India was in the range between 0.4 to 71.87%, 0.14 to 42% and 0.3 to 29.57%, respectively (Jayaram et al., 2021) This relative difference in the prevalence of the three STHs is observed similarly across all regions of all countries and has been persistent even prior to independent review studies. The current study also suggests the prevalence of Ascaris lumbricoides as the highest in northern Nigeria; this can be attributed to ownership of domestic animals and improper hand-washing practices, especially after defecating. In contrast, another study showed a decreasing trend in prevalence for A. lumbricoides, and T. trichiura (6·6%, and 4·4%) among school-aged children from 2000 onwards in sub-Saharan Africa (Sartorius et al., 2020).

Table 8: Authors Recommendations on STH Infections in northern Nigeria

Out of 9.384 (51.5%), males had the highest infection rate PPE of 1,880 (59.5%, 95% CI: 58.1- 60.1), and females had 1,280 (20.5%, 95% CI: 19.1–21.1). Gender distribution is not a confounding factor in STH infections, as both sexes are equally susceptible. Data from the reviewed literatures show more than one-third of the Ethiopian SAC were infected with STH, a close margin and insignificant gender difference between in Southwest and Northcentral regions (Samuel, 2015; Leta et al., 2020).

The studies used a variety of age intervals; consistent age-group intervals were 3, 4, and 5 (75.8%). Age-highest PPE of 88.0% was recorded between 6 – 17 years, and the lowest PPE of 0.0% was recorded in older children between the ages of 16 -20 years. Additionally, two studies reported that older children were more likely to be parasitized with STH than their younger counterparts(Abe et al., 2019; Dawaki et al., 2019) Children aged 5–14 years are known to carry the heaviest burden of soil-transmitted helminthiasis, this is in line with the findings of the association of high STH infections with children aged 2–5 years in northern Nigeria (Shuaibu et al., 2018; Taiwo et al., 2019) Age group of 4–10 years is the high-risk group and most STH infected children (Ishaku et al., 2020).

The identified risk factors associated with STH infections in northern Nigeria include drinking untreated water 12 (44.4%); OR 1.66 (95% CI: 1.30 - 19.49) p=0.53, open field or bush defecation 8 (29.6%); OR 3.41 (95% CI: 1.94 - 9.32) p=0.72, walking barefooted 6(22.2%); OR 1.16 (95% CI: 1.53 - 6.42) p=0.44 Not wearing shoes can increase the risk of infection with STH that penetrates the skin to infect humans (Brahmantya et al., 2020; Khan et al., 2022) Eating unwashed fruits and/or vegetable 1 (3.7%); OR 2.01 (95% CI: 1.32 - 4.51) p=0.54. Consumption of raw vegetables is known to increase the risk of exposure to STH eggs if they are not appropriately cleaned due to the possibility of contamination of STH eggs from the soil (Kiiti et al., 2020). The most recent study examining risk factors for STH in Honduras showed that the number of children in the household with a recent history of diarrhea was associated with ascariasis caused by improper hygiene (Sanchez et al., 2014). Patterns of soil-transmitted helminth infection in sub-Saharan Africa have changed, and the prevalence of infection has declined substantially in this millennium, probably due to socioeconomic development and large-scale deworming programs (Mackinnon et al., 2019).

CONCLUSION

STH infections are highly prevalent and well distributed across Nigeria and within community settings. This systematic literature review comprehensively overviews soil-transmitted helminth infections in northern Nigeria. The findings underscore the urgent need for improved surveillance, targeted interventions, and enhanced healthcare infrastructure to control and manage STH infections in this region. The data presented in this review can serve as a valuable resource for policymakers, healthcare professionals, and researchers working towards the eradication of STH infections in northern Nigeria. Furthermore, the identified research gaps call for further studies to enhance our understanding of the epidemiology and control of STH infections in northern Nigeria. Additional research is warranted to address existing gaps, such as the impact of STH infections on maternal and child health, the efficacy of different control measures, and the economic burden of these infections.

RECOMMENDATIONS

School Health Services are recommended in all primary and Secondary schools; regular deworming and provision of portable drinking water, sanitation and improved personal hygiene, regular health education and potable drinking water, as well as the implementation of sustainable intervention measures, were the common recommendations made by the authors.

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