Soil-transmitted helminth infection among school-age children in Ogoja, Nigeria: implication for control

doi:10.21203/rs.3.rs-2104583/v1

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Soil-transmitted helminth infection among school-age children in Ogoja, Nigeria: implication for control

https://doi.org/10.21203/rs.3.rs-2104583/v1

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published 08 Mar, 2023

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The study aimed at assessing the prevalence and risk factors of soil-transmitted helminthiases amongst school-aged children in Ogoja Local Government Area, Cross River State. Faecal samples were collected from 504 participants and analysed using the Kato-Katz technique. A total of 232 (46.0%) samples were positive for soil-transmitted helminths. The overall prevalence of Ascaris lumbricoides, hookworm, Trichuris trichiura, and Strongyloides stercoralis were 14.1%, 16.5%, 2.6%, and 12.9% respectively. The prevalence of infections were higher among males (46.6%) than females (45.4%). Overall parasitic infection was higher in the 5–7 year age group (65.6%) than in the other age groups (p = 0.000). Infection intensities of A. lumbricoides (84.00 EPG) (p = 0.044) and T. trichiura (96.00 EPG) (p = 0.041) were higher in school-age children aged 14–16 years. A. lumbricoides and hookworm co-infection (8.7%) was the most common mixed infection and was significantly higher in males than females. School-aged children who did not have prior knowledge about soil-transmitted helminth infections, the habit of drinking water without boiling, open defecation, use of pit latrine and children who did not have toilet facilities in school were significantly associated with soil-transmitted helminthiases. There was a significant relationship between washing hands after using the toilet, the habit of putting on footwear outside the house, and soil-transmitted helminth infection. In addition to preventive chemotherapy, control measures should focus on health education, providing clean drinking water, proper disposal of human excreta and sewage, and environmental hygiene.

Soil-transmitted helminths

School-age children

School attendance

Ascaris lumbricoides

Hookworm

Nigeria

In Sub-Saharan Africa, considerable morbidity and death are brought on by soil-transmitted helminthiases. According to estimates, soil-transmitted helminth infections affect more than 1.5 billion people globally (WHO 2019). According to estimates, 198 million people in sub-Saharan Africa carry hookworm infections, 173 million suffer from ascariasis, and 162 million have trichuriasis (Molyneux et al. 2005).

Soil-transmitted helminthiases caused by the roundworm (Ascaris lumbricoides), the whipworm (Trichuris trichiura), and two Hookworm species (Ancylostoma duodenale and Necator americanus) are listed among Neglected Tropical Diseases (NTD) (Hotez et al. 2006). It has been established that these helminths are associated with chronic, disabling, and disfiguring conditions occurring in settings of extreme poverty and poor sanitation (Rujeni et al. 2017). The occurrence of soil-transmitted helminthiases is associated with factors such as limited access to clean water, ignorance of simple health-promoting factors, tropical climate, and low altitude (WHO 2002). According to reports, areas with a high level of poverty, poor or nonexistent sanitation, and a need for increased health education and treatment are those where soil-transmitted helminthiases are most prevalent and severe (Andrea et al. 2012). In most developing nations, including Nigeria, these variables are prevalent and predominant, especially in rural settings, urban slums, and high-density regions.

Studies carried out in Nigeria and globally on soil-transmitted helminthiases have described ascariasis as the most prevalent, followed by hookworm infections and trichuriasis (Hotez and Kamath, 2009; Karshima 2018). School-aged children are most severely infected (Obeta et al. 2019), and their growth and physical fitness, school attendance, and cognitive performance are greatly affected (Gimba and Dawan 2015).

To combat soil-transmitted helminthiasis, the World Health Organization approved preventive chemotherapy with albendazole/mebendazole in 2001. The main element of this plan was the routine prescription of antihelmintic medications to at-risk populations, including children, women of reproductive age, and individuals in high-risk jobs including farming and night-soil reuse (WHO, 2006). Although this approach reduces disease, investigations have shown that it does not stop significant reinfections (Jia et al. 2012; Ziegelbauer et al. 2012).

Soil-transmitted helminths are still a public health problem despite several treatment initiatives and regulations at the national level by the government of Nigeria and other partners in the health sector in Nigeria and elsewhere. In Nigeria, the National Soil-transmitted Helminths Control Programme was initiated in 2007. This programme benefits from Mebendazole donations from Merck KGAe Germany and Johnson and Johnson. Targeted treatments with this drug are currently ongoing in Cross River State and Nigeria at large (Federal Ministry of Health 2015). Additionally, in 2016, the Cross River State Ministry of Health's Neglected Tropical Diseases (NTD) unit launched its inaugural state-wide school-based deworming exercise for soil-transmitted helminthiases. However, it has been noted that in Nigeria, there is a considerable sustained prevalence of soil-transmitted helminthiases despite the chemotherapy strategies put in place (Karshima 2018). School-aged children in the study area, who are the most susceptible demographic, have received very little attention when it comes to the identification of risk factors for soil-transmitted helminth infection (WHO 2009). Integrated control strategies that incorporate access to sanitation, health education, and other complementary primary preventive measures are required to interrupt the spread of the disease and achieve local helminthiasis eradication (Ziegelbauer et al. 2012).

This study therefore aimed at assessing the prevalence and risk factors of soil-transmitted helminthiases amongst school-aged children in Ogoja Local Government Area, Cross River State. This will help in preferring suitable and sustainable control measures for eliminating soil-transmitted helminthiases in the study area.

Study site

The research was carried out in Ogoja Local Government Area (LGA), Cross River State, Nigeria (Figure 1). Ogoja is 830 feet above sea level and is situated in Latitude 6⁰39'17" North and Longitude 8⁰47'51" East. Ogoja town shares boundaries to the North and West with Yala LGA, to the Northeast with Bekwarra LGA, to the East with Obudu and Boki LGAs, and to the South with Ikom LGA (NPC 2006). The region normally has a tropical climate with two distinct seasons: dry (November to March) and wet (April to October). The region has an average annual temperature of 27°C and 1200 mm of precipitation. Farming is the main occupation with the rest of the population comprising artisans, transport workers, traders, and civil servants. Although there are few public water and private boreholes available, inhabitants still depend on streams as a major source of water.

Study design

This study employed a cross-sectional design and was carried out between January and March 2021. It targeted school-age children aged 5 to 16 years from primary and secondary schools in Ogoja Local Government Area, selected using the simple random sampling method. Only after the study's objective had been communicated to the respondents, their parents, or other legal guardians, were they encouraged to participate in the study. Only respondents who had taken a deworming drug within the last year were examined. Faecal samples were obtained from all respondents.

A total of seven schools were selected from Mbube and Nwang communities namely, Ntol Comprehensive Secondary School, Ndok, Government Migrant Science and Technology College, Mbube, Christ the King Primary School, Mbube, Abi Iruan Primary School, Mbube, Community Primary School, Eshanjok, Community Secondary School, Nwang and Saint Theresa Community Primary School, Nwang.

Sample size determination

The sample size for this study was estimated using the formula described by Bruno and Omar (2016), N = Z² (PQ/I²) where: N = sample size, I = 0.05 (margin error), q = 1 – p, z = standard normal deviation set at 1.96 for 5% significance level and p = baseline prevalence of urinary schistosomiasis and soil-transmitted helminthiasis co-infection (45%) (Federal Ministry of Health 2015). The determined minimum sample size was 380. To account for potential issues like data loss and participant withdrawal, a total of 504 participants were enrolled for this study.

Examination of faecal samples for soil-transmitted helminths

Properly labeled specimen containers with tight lids for collecting fresh faecal samples and an applicator stick were provided for each participant. Faecal samples were preserved in 10% formaldehyde before transportation to the laboratory for parasitological analysis.

The specimens collected were examined using the Kato Katz techniques described by Aribodor et al. (2018). Two hundred milligrams of the faecal sample were transferred from the labeled plastic container and placed on a piece of newspaper. Part of the faeces was sieved through the screen by applying pressure on the top with a piece of wire gauze. The sieved faeces were transferred to fill the hole in the template after a standard template was put on the slide. After that, the template was gently taken off, leaving a slide with a cylinder of feces weighing around 41.7 mg. Then, a cellophane strip that had already been soaked in Lugol's solution was used to cover it. To distribute uniformly, the slide was reversed and firmly placed on the cellophane strip. The slide was then put on a microscope slide rack and left for 40 to 60 minutes to dry and clear. The slide was then examined under a light microscope at 10× and 40× objective lenses. Ova of intestinal helminths were identified using keys provided by Cheesebrough (2000) and counted. By multiplying the total number of eggs counted by a multiplication factor of 24, the egg per gram (EPG) faecal value was determined (Aribodor et al. 2018). According to WHO recommendations, infection intensities were divided into three categories: low, moderate, and heavy (WHO 2002).

Knowledge attitude and practices (KAP)

The Knowledge, Attitude, and Practice (KAP) of school-age children concerning worm infestations, their causes and effects, and the general sanitary behaviour in the communities were evaluated through structured questionnaires.

Issues on home socio-demographics were covered by the questionnaire. Personal hygiene, environmental sanitation information, practices, knowledge of common signs and symptoms, mode of transmission, treatment, and control of soil-transmitted helminthiasis among school-age children in the selected schools were also covered. All questionnaires were properly labeled with each participant’s identification number.

School attendance

Along with each respondent's parasitological information, the head teacher or administrator of each school recorded each student's attendance. Regular school attendance was defined as being present on the majority of instructional days, whereas irregular attendance was defined as being absent on the majority of instructional days.

Data analysis

The SPSS program version 22 was used for statistical analysis of the data. The prevalence and severity of infections were determined using descriptive statistics. The connections and discrepancies between the data on factors and the outcomes from sample examinations were evaluated using the chi-square test. To compare the average infection intensity by egg count in the various variables, analysis of variance (ANOVA) was utilised. The strength of the connection between co-variables and soil-transmitted helminthiases was assessed using an odds ratio (OR) with a 95% confidence interval (CI). Graphs were created using Prism GraphPad version 5 and Microsoft Excel (GraphPad Software, La Jolla, USA). Statistical significance was set at P < 0.05.

Demographic characteristics of study participants

A total of 504 school-age children were screened for soil-transmitted helminthiases. Of these, 253 (50.2%) were males while 251 (49.8%) were females. For the age categories of 5-7 years, 8-10 years, 11-13 years, and 14-16 years, respectively, the age distribution of the study participants was 32 (6.3%), 178 (35.3%), 223 (44.2%), and 71 (14.1%) (Figure 2).

Prevalence of soil-transmitted helminthiases among school-age children

Five hundred and four (504) faecal samples were examined for soil-transmitted helminthiases. Two hundred and thirty-two [232/504, (46.0%)] samples were positive for soil-transmitted helminths (Table 1). Four species of helminths namely, Ascaris lumbricoides, hookworm, Trichuris trichiura, and Strongyloides stercoralis were recovered from the school children investigated. The overall prevalence of Ascaris lumbricoides, Hookworm, Trichuris trichiura, and Strongyloides stercoralis was 14.1%, 16.5%, 2.6%, and 12.9% respectively (p=0.000) (Table 1).

Table 1: Prevalence of soil-transmitted helminthiases among school-age children according to schools surveyed in Ogoja Local Government Area.

Schools	Number examined	Hookworm n (%)	A. lumbricoides n (%)	T. trichiura n (%)	S. stercoralis n (%)	Overall Infection (%)	P value
Ntol Comprehensive Secondary School	72	9 (12.5)	5 (6.9)	3 (4.2)	6 (8.3)	23 (31.9)	0.353
Government Migrant Science and Technology College	70	11 (15.7)	7 (10.0)	2 (2.9)	9 (12.9)	29 (41.4)	0.104
Christ the King Primary School, Ndok	69	17 (24.6)	12 (17.4)	3 (4.3)	6 (8.7)	38 (55.1)	0.006
Abi Iruan Primary School	74	16 (21.6)	12 (16.2)	1(1.4)	15 (20.3)	44 (59.5)	0.005
Community Primary School, Eshanjok	66	9 (13.6)	13 (19.7)	1 (1.5)	12 (18.2)	35 (53.0)	0.017
Community Secondary School, Nwang	70	12 (17.1)	14 (20.0)	2 (2.9)	9 (12.9)	37 (52.9)	0.030
St. Theresa Community Primary School, Nwang	83	9 (10.8)	8 (9.6)	1 (1.2)	8 (9.6)	26 (31.3)	0.002
Total	504	83 (16.5)	71 (14.1)	13 (2.6)	65 (12.9)	232 (46.0)	0.000
P Value		0.046	0.001	0.584	0.366	0.125

The highest prevalence of Ascaris lumbricoides (20.0%) and hookworm (24.6%) were recorded in Community Secondary School, Nwang, and Christ the King Primary School, Ndok, respectively. For Strongyloides stercoralis infection, the highest prevalence (20.3%) was recorded in Abi Iruan Primary School. Ntol Comprehensive Secondary School recorded the lowest prevalence of both A. lumbricoides and S. stercoralis infections (6.9% and 8.3% respectively). St. Theresa Community Primary School, Nwang, recorded the lowest prevalence of hookworm (10.8%). Infections with Trichuris trichiura were generally low across the different schools when compared with other parasitic infections observed (Table 1).

School-age children from Abi Iruan Primary School, recorded the highest prevalence of infection (59.5%) although this was not significantly different (p=0.125) from infections recorded in other schools. Parasitic infections varied significantly (P<0.05) in Christ the King Primary School, Ndok, Abi Iruan Primary School, Community Primary School, Eshanjok, Community Secondary School, Nwang, and St. Theresa Community Primary School, Nwang, with relatively high levels of hookworm and Ascaris lumbricoides infections compared to other infections recorded (Table 1).

The prevalence of infections among males (46.6%) and females (45.4%) was very close and showed no significant variation (p=0.793) (Figure 3). The prevalence of hookworm (16.6%), Ascaris lumbricoides (14.6%), and Trichuris trichiura (3.6%) were higher in males than in females. However, females recorded a higher prevalence of Strongyloides stercoralis (13.9%) infection. The results also revealed that overall parasitic infection was higher in the 5-7 year age group (65.6%) than in the other age groups (p=0.000) (Figure 3). The age group with the lowest prevalence was 11-13 years, with a rate of 35.9%. Hookworm, Ascaris lumbricoides, and Trichuris trichiura infections were highest (20.8%, 19.7%, and 3.4%, respectively) among school-aged children in the 8-10 year age group compared with other age groups. Hookworm, A. lumbricoides, and S. stercoralis infections varied significantly across the age groups (P<0.05) (Figure 4).

The intensity of soil-transmitted helminthiasis

Overall, the mean parasite loads for Ascaris lumbricoides, hookworm, and Trichuris trichiura were 80.11, 90.23, and 44.31 eggs per gram (EPG), respectively. The intensity of hookworm (90.60 EPG) (p=0.941) and Trichuris trichiura (45.33 EPG) (p=0.810) infections were observed to be higher in males, except for Ascaris lumbricoides (84.00 EPG) infection, which was higher in females (p=0.399) (Figure 5). Between the age groups, the infection intensities of A. lumbricoides (84.00 EPG) (p=0.044) and T. trichiura (96.00 EPG) (p=0.041) were significantly higher in school-age children aged 14-16 years. The intensity of hookworm (96.00 EPG) infection was higher in school-aged children aged 5-7 years than in other age groups (p=0.145) (Figure 6). All participating school-age children had light infections according to WHO classification.

Prevalence of multiple infections of soil-transmitted helminths

Ascaris lumbricoides and hookworm co-infection (8.7%) was the most common mixed infection encountered in the study and were significantly higher in males than females (p=0.035) (Table 2). Ascaris lumbricoides, Trichuris trichiura, and Strongyloides stercoralis co-infection (0.4%) together with A. lumbricoides, hookworm, and S. stercoralis (0.4%) co-infection were the least frequently encountered multiple infection categories and only occurred in males. Males generally had a higher prevalence than their female counterparts in all multiple infection categories except for hookworm and S. stercoralis co-infection (1.2%) (Table 2).

Factors associated with soil-transmitted helminthiases among school-age children

Out of 504 school-age children screened for soil-transmitted helminth infections, 355 responded/filled the questionnaires accurately, giving a response rate of 70.4%.

School-aged children with no prior knowledge of soil-transmitted helminth infections were 1.918 times more likely (OR = 1.918, 95% CI: 0.195 – 0.576) (p=0.000) to be infected with soil-transmitted helminths. The habit of treating water by boiling it before drinking was significantly associated with soil-transmitted helminth infections. Children who did not treat water before drinking were approximately 3 times at higher risk of infection with soil-transmitted helminths (OR= 3.250, 95% CI: 0.213 – 0.840) (p=0.014) (Table 3).

Compared with children who used flush toilets, children who defecated openly were more likely to be infected with soil-transmitted helminths (OR=26.495, 95% CI: 7.857 – 89.355) (p=0.000). Additionally, school children who used pit latrines were 4 times more likely to be infected with soil-transmitted helminths (OR = 4.159, 95% CI: 1.252 – 13.812) (p=0.000).

Table 2: Prevalence of multiple infections of soil-transmitted helminthiases by gender among school-age children examined in Ogoja Local Government Area.

	Male (n = 253)	Female (n = 251)	Total (N = 504)	P value
Parasite	No. (%) infected	No. (%) infected	No. (%) infected
Ascaris lumbricoides + Hookworm	29 (11.4)	15 (5.9)	44 (8.7)	0.035
Ascaris lumbricoides + Trichuris trichiura	5 (1.9)	2 (0.8)	7 (1.4)	0.257
Hookworm + Trichuris trichiura	4 (1.6)	1 (0.4)	5 (0.9)	0.180
Ascaris lumbricoides + Strongyloides stercoralis	8 (3.2)	7 (2.8)	15 (2.9)	0.796
Hookworm + Strongyloides stercoralis	2 (0.8)	3 (1.2)	5 (0.9)	0.655
Ascaris lumbricoides + Trichuris trichiura + Strongyloides stercoralis	1 (0.4)	0 (0)	1 (0.4)	NA
Ascaris lumbricoides + Hookworm + Trichuris trichiura	4 (1.6)	2 (0.8)	6 (1.2)	0.414
Ascaris lumbricoides + Hookworm + Strongyloides stercoralis	1 (0.4)	0 (0)	1 (0.4)	NA

The likelihood of infection with soil-transmitted helminths was higher in children who did not have toilet facilities in school (OR = 2.423, 95% CI: 0.328 – 0.923) (p=0.024). There was a significant relationship between washing hands after using the toilet, the habit of putting on footwear outside the house, and soil-transmitted helminth infection (P<0.05) (Table 3).

Children with soil-transmitted helminth infections were more likely to have parents/guardians who had no formal education (OR = 2.176, 95% CI: 0.790 – 6.000). Unemployed parents/guardians (OR = 2.011, 95% CI: 0.492 – 8.211) had children who were approximately 2.0 times more likely to be infected with soil-transmitted helminths than those who had formal employment. School children who attended school regularly were less likely to be infected with soil-transmitted helminth (OR = 0.200, 95% CI: 0.078 – 0.512) (p=0.001) (Table 4).

Table 3: Prevalence and factors associated with soil-transmitted helminthiases infection in Ogoja Local Government Area

Variables	No. examined (%) n= 355	No. Negative (%)	No. Positive (%)	OR (CI, 95%)	P value
Heard about soil-transmitted helminths
Yes	286 (80.6)	188 (65.7)	98 (34.3)	1
No	69 (19.4)	27 (39.1)	42 (60.9)	1.918 (0.195 – 0.576)	0.000
Treat water before drinking (boiling)
Yes	51 (14.4)	39 (76.5)	12 (23.5)	1
No	304 (85.6)	176 (57.9)	128 (42.1)	3.250 (0.213 – 0.840)	0.014
Toilet facility
Flush toilet	124 (34.9)	120 (96.8)	4 (3.2)	1
Pit latrine	122 (34.4)	74 (60.7)	48 (39.3)	4.159 (1.252 – 13.812)	0.000
Open defecation	109 (30.7)	21 (19.3)	88 (80.7)	26.495 (7.857 – 89.355)	0.000
Toilet in school
Yes	89 (25.1)	63 (70.8)	26 (29.2)	1
No	266 (74.9)	152 (57.1)	114 (42.9)	2.423 (0.328 – 0.923)	0.024
Wash hands after using the toilet (water)
Yes	12 (3.4)	2 (16.7)	10 (83.3)	1
No	343 (96.6)	213 (62.1)	130 (37.9)	8.192 (1.767 – 37.977)	0.007
Put on footwear outside the house
Throughout	52 (14.6)	40 (76.9)	12 (23.1)	1
Seasonally	197 (55.5)	119 (60.4)	78 (39.6)	2.185 (1.079 – 4.424)	0.030
Once in a while	98 (27.6)	51 (52.0)	47 (47.9)	3.072 (1.441 – 6.550)	0.004
Never	8 (2.3)	5 (62.5)	3 (37.5)	2.000 (0.416 – 9.613)	0.387

Table 4: Prevalence of soil-transmitted helminthiases by the level of education, occupation of the parents, and school attendance among school-age children in the study

Variables	No. examined (n=355)	No. Negative (%)	No. Positive (%)	OR (CI, 95%)	P value
Level of education
No formal education	48 (13.5)	11 (22.9)	37 (77.1)	2.176 (0.790 – 6.000)	0.133
Primary education	88 (24.8)	63 (71.6)	25 (28.4)	0.257 (0.106 – 0.624)	0.003
Secondary education	191 (53.8)	130 (68.1)	61 (31.9)	0.304 (0.134 – 0.687)	0.004
Post-secondary education	28 (7.9)	11 (39.3)	17 (60.7)	1
Occupation
Farmers	293 (82.5)	201 (68.6)	92 (31.4)	0.162 (0.078 – 0.337)	0.000
Unemployed	20 (5.6)	3 (15.0)	17 (85.0)	2.011 (0.492 – 8.211)	0.331
Formal employment	42 (11.8)	11 (26.2)	31 (73.8)	1
School attendance
Regular	176	96 (54.5)	80 (45.5)	0.200 (0.078 – 0.512)
Not regular	31	6 (19.4)	25 (80.7)	1	0.001
Total	207	102 (49.3)	105 (50.7)

The findings from this study show that Ogoja Local Government Area (LGA) in Cross River State is endemic for soil-transmitted helminth infections. The overall prevalence of soil-transmitted helminthiasis (STH) (46.0%) falls within the stipulated range among Local Government Areas of Cross River State (12.5–50.2% for soil-transmitted helminthiases), as previously reported by the Nigerian Federal Ministry of Health (Federal Ministry of Health 2015). However, after three rounds of Mass Drug Administration (MDA) of albendazole in the study area, the overall prevalence of STH (46%) was higher than the 12.7% reported for Ogoja LGA by the Cross River State Neglected Tropical Disease survey in 2018. This shows that despite the ongoing deworming exercise, soil-transmitted helminth infections are still maintained in the population. Jia et al. (2012) reported that after mass drug administration, the prevalence of STH infections recovers rapidly, especially in endemic areas. This further highlights the fact that there are factors that contribute to the reinfection of treated individuals with the disease within the study area. Before 2019, there were three rounds of treatment with albendazole for STH infections among school-age children in the study area. The focus on school-age children means that out-of-school children and community members are often left out during Mass Drug Administration. These groups could serve as sources of reinfection of treated individuals within the community.

The high prevalence of STH (46%) seen in this study is consistent with findings from prior studies conducted in Nigeria and other regions of Africa. In Enugu state, schoolchildren had a prevalence of 49.6%, according to Aribodor et al. (2018). Agbolade et al. (2007) and Salawu et al., (2014) reported a prevalence of 66.2% and 62.2% among school-age children in Ogun and Oyo states respectively. Additionally, in Northwest Ethiopia, schoolchildren showed a prevalence incidence of 51.5%, according to Abera et al. (2013). Current socioeconomic and environmental variables may be connected to this high prevalence of STH.

Hookworm was the most prevalent among the soil-transmitted helminths (16.5%), followed by Ascaris lumbricoides, S. stercoralis, and Trichuris trichiura. This aligns with mapping results conducted in Ogoja Local Government Area in 2014, which reported hookworm (11.51%) as the most prevalent soil-transmitted helminth, followed by T. trichiura (1.19%) and A. lumbricoides (0.4%). Hookworm infection is influenced by habits such as not wearing footwear regularly (Alelign et al. 2015). This was observed among the school-age children recruited for the study, coupled with the fact that some areas around the schools visited were used as toilets by the children, thus exposing them to hookworm infestation. Reports have also shown that individuals in agrarian communities are at a greater risk of Hookworm infection (Ukibe et al 2018). Similar findings have been reported by Alelign et al. (2015). Alelign et al. (2015) in Ethiopia reported the prevalence of hookworm infection to be significantly higher than infection with other soil-transmitted helminths in school children and this was attributed to the fact that most children studied did not wear shoes and walked over loamy soils and cultivated fields. In contrast, most studies on soil-transmitted helminth infections especially in endemic countries, have identified A. lumbricoides as the most common infection (Lai et al. 2013; Schule et al. 2014; Oluwole et al. 2018). This was ascribed to the A. lumbricoides ova's capacity to endure adverse environmental circumstances in the soil until advantageous conditions for embryonation were available.

Strongyloides stercoralis infection has been reported in separate studies (Al-Mekhlafi et al. 2017; Karshima 2018). The prevalence of 12.9% recorded in this study is similar to that reported by Al-Mekhlafi et al. (2008) in Malaysia (15.8%). It was reported that the laboratory technique used in analysing stool samples had an impact on the number of S. strongyloides larvae seen. Additionally, walking barefoot and bathing in rivers/streams were associated with strongyloidiasis (Morales et al. 2019).

Infections with Trichuris trichiura were generally low when compared with other parasitic infections observed. A low prevalence of T. trichiura infection has been reported elsewhere by Ukpong and Agamse (2018) and Usang et al (2020). The investigation was conducted during the dry season when the environment becomes unfavourable for the formation of T. trichiura ova in the soil, which accounts for the low prevalence (Brooker and Michael 2000).

The overall prevalence of infections among males and females was very close and showed no significant difference. This shows that school-age children are exposed to a similar risk of infection by these helminths. Similar results have been reported by Ntonifor et al. (2015) in Cameroon and Salawu et al. (2014) in Nigeria. However, the prevalence of A. lumbricoides (14.6%), hookworm (16.6%), and T. trichiura (3.6%) were higher in males than in females. Oyibo et al. (2011), in a study in Ebonyi, reported helminth infection to be significantly higher in males than in females but suggested that more studies should be done to ascertain whether helminth infection is gender-dependent. In contrast, Nkengazong et al. (2010) in Cameroun reported a high prevalence of A. lumbricoides and T. trichiura in females compared to males and attributed this to different patterns of soil contact.

The results also revealed that overall parasitic infection was higher in the 5–7 year age group (65.6%) than in other age groups. This agrees with the results reported by Salawu and Ughele (2015) and Ukibe et al. (2018) in Nigeria. Children in this age group 5–7 are active and play indiscriminately with materials and edibles. In contrast, Alemu et al. (2019) and Alelign et al. (2015) in separate studies, reported that school-age children within the age group of 10–14 years are engaged more in agricultural activities and are more active than younger children; therefore, they are at a higher risk of acquiring parasitic infections. A. lumbricoides (19.7) and T. trichiura (3.4%) infections were highest among school-aged children in the 8–10 year age-group compared with other age-groups, which hints to the energetic character of children in this age range who spend a lot of time playing, exposing themselves to a high risk of infection. Atta et al. (2018) stated that older children are more independent and that as such, their hygiene is less likely to be monitored by their parents. However, Aribodor et al. (2018) showed a greater prevalence of A. lumbricoides and hookworm infection in children between the ages of 4 and 7 and claimed that due to their active behaviour, children under this age are more likely to come in touch with contaminated soil.

The presence of multiple helminth infections has been reported in school-age children in Nigeria and Uganda (Ojja et al. 2018; Ukpong and Agamse 2018, Awharitoma et al. 2020). The most typical mixed infection found in the study was Ascaris lumbricoides and hookworm co-infection, with a prevalence of 8.7%. This is consistent with the findings of Agbolade et al. (2007) and Salawu and Ughele (2015), who claimed that the most frequent concurrent infection among school-age children in southwestern Nigeria was A. lumbricoides and hookworm. In contrast, Nkengazong et al. (2010) in Cameroon reported A. lumbricoides and T. trichiura (95.6%) to be the most frequently encountered co-infections in the sampled population. The majority of helminthic infections in Africa, according to studies, occur as co-infections rather than as isolated infections (Salawu et al. 2014). This is supported by common epidemiological factors that enhance the spread of these diseases.

Mixed infections were significantly higher in males, and Yu et al. (2017) reported a similar result in a study done in Northern Samar, Philippines. Co-infection of soil-transmitted helminths has been shown to affect morbidity as reported by Rujeni et al. (2017) in Rwanda and this can have serious socioeconomic consequences on households.

All participating school-age children had light soil-transmitted helminthiasis infections according to the WHO classification (WHO 2002). This reflects positively on the ongoing deworming programmes, indicating positive effects concerning infection burden. This shows that the continuous treatment of school-age children will further reduce the parasitic egg burden and subsequently the prevalence of the disease. Low-intensity soil-transmitted helminth infections have been reported by Pasaribu et al. (2019) in Indonesia and Awharitoma et al. (2020) in Nigeria. In a study in Yemen, Al-Mekhlafi et al. (2016) noted that low intensities of soil-transmitted helminth infections may still harm children's health and quality of life.

The intensity of hookworm and Trichuris trichiura infections was observed to be higher in males, except for infection with A. lumbricoides which was higher in females. However, none of these changes were statistically significant. According to Ojja et al. (2018), more study is required to investigate the possible causes of the observed gender disparities in the severity of helminth infection among school-age children.

In this study, factors connected to soil-transmitted helminth infections were found. In locations where soil-transmitted helminthiases are prevalent, socioeconomic variables such as a lack of potable water, employment, and attitudes such as improper sewage disposal and inadequate sanitation have been identified as determining factors (Bethony et al. 2006).

Knowledge, attitude, and practices were determinants of soil-transmitted helminth infection in the study area. School-age children who did not have prior knowledge about soil-transmitted helminth infections were 1.918 times more likely to be infected with soil-transmitted helminths than those who had heard about soil-transmitted helminths. Poor knowledge about soil-transmitted helminth infections increases the risks of infection as individuals are unaware of the factors that expose them to the infection. Ojja et al. (2018) also reported inadequate knowledge about the transmission and prevention of soil-transmitted helminths as factors associated with the infection.

The habit of treating water by boiling it before drinking was significantly associated with soil-transmitted helminth infections. Children who did not treat water before drinking was 3 times at higher risk of infection with soil-transmitted helminths compared to those having the habit of boiling water before drinking. Echazu et al. (2015) noted that unimproved drinking water was significantly associated with increased odds of infection with orally ingested soil-transmitted helminths. Sugianto et al. (2019) in a study carried out in Bali, also pointed out that the source of water from rivers is the dominant risk factor for soil-transmitted helminth infection.

The likelihood of infection with soil-transmitted helminths in children who did not have toilet facilities in school was higher than that in children who did. This was expected as the schools visited in the study area had substandard or no toilets available. This leads to indiscriminate defecation by school children in the school surroundings exposing them to infections with soil-transmitted helminths. As shown in this study, children who defecated openly were more likely to be infected with soil-transmitted helminths. When present, the toilet facilities were in poor condition and the study showed that toilet type significantly influenced the likelihood of school children being infected with soil-transmitted helminths.

The habit of putting on footwear outside the house was significantly associated with soil-transmitted helminth infection. This is especially clear in the case of hookworm infection since the infective stages of this parasite grow close to the places where people defecate, where the eggs are discharged and may infect an unwitting host. Children are more likely to roam about barefoot in rural settings, as this study has shown, which puts them at risk of coming into contact with contaminated soil and helminth infection. This agrees with reports from Nigeria and India (Kattula et al. 2014; Alelign et al. 2015; Anunobi et al. 2019). By promoting health and providing water closet systems, open defecation may be eliminated.

The odds of acquiring soil-transmitted helminth infections by children who did not wash their hands were 8 times higher than those who did. According to Alemu et al. (2019), children who do not wash their hands after going to the bathroom were about 4.5 times more likely to acquire soil-transmitted helminth infections.

Although not statistically significant, children whose parents/guardians had no formal education were approximately 2 times more likely to be infected with soil-transmitted helminths than children whose parents/guardians had postsecondary education. It has been reported that a low level of education is a reliable indirect indicator of soil-transmitted helminth infections (Ross et al. 2017). In contrast, Alelign et al. (2015) found no connection between schoolchildren's exposure to soil-transmitted helminth infections and the education level of parents or guardians in Durbete town, Northwest Ethiopia.

Unemployed parents/guardians had children who were also approximately 2.0 times more likely to be infected with soil-transmitted helminths than those who had formal employment. Salawu and Ughele (2015) reported parental socioeconomic status to be an important variable in determining risk factors predisposing school-age children to soil-transmitted helminth infection. It was stated that school-age children whose parents were farmers were 3.0 times more likely to be infected when compared with others whose parents were civil servants. It was explained that children who often carried out agricultural activities with their parents were exposed to contaminated soil, particularly where night soil is used as fertilizer for crops.

Additionally, it has been noted that helminth infection has an impact on school attendance since infected children are more prone to miss school (WHO 2002). Findings from the study show that the prevalence of soil-transmitted helminths was significantly associated with children who did not attend school regularly. This can be linked to the high prevalence of soil-transmitted helminth infections in the study, although the intensities of infections were low. The implication of this is that fewer school-age children will receive treatment for soil-transmitted helminth infections, as most treatment programmes are school-based (De Clercq et al. 1998).

The findings from this study show that Ogoja Local Government Area in Cross River State is still endemic to soil-transmitted helminthiasis despite ongoing deworming programmes. Although the intensity of soil-transmitted helminth infection was typically low, urgent integrated control efforts are still required to eliminate helminth infection in the study area. These actions should prioritize hand-washing with soap, providing clean drinking water, disposing of human waste and sewage properly, and educating people about public health. The importance of environmental hygiene and sanitation is a very important indicator in the control of helminth infection.

Funding

No funding was received for conducting this study.

Conflicts of interest/Competing interests

The authors have no competing interests to declare that are relevant to the content of this article.

Data availability

All datasets generated for this study are included in the article.

Author contributions

Edema Enogiomwan Imalele participated in the formal analysis and investigation, data analysis, writing, and editing of the original draft manuscript. Emmanuel Offiong Effanga participated in the formal analysis and investigation, writing, and editing of the draft manuscript. Ekanem Ikpi Braide planned the study research, and edited the original draft manuscript. Ubleni Etta Emanghe collaborated in editing of the draft manuscript. Anok Ukam Usang participated in the data analysis, writing, and editing of the draft manuscript.

Ethics approval

Ethical clearance was obtained from the Ministry of Health, Health Research Ethics Committee, Cross River State (CRS/MH/HREC/018/Vol.V1/149).

Consent to participate

Principals and headmasters/headmistresses of participating schools were informed, and the nature of the study was explained. Permission to carry out the study was subsequently obtained. Informed consent was obtained from parents/guardians of participating school-age children and all individual participants included in the study.

Consent for publication

Not applicable

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No competing interests reported.

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Soil-transmitted helminth infection among school-age children in Ogoja, Nigeria: implication for control

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