Soil-transmitted helminth infections and nutritional indices among children (5–9 years) and adolescents (10–12 years) in Calabar, Nigeria

Abstract

Background

Soil-transmitted helminth (STH) infections are a significant public health concern in developing countries, particularly affecting children (5–9 years) and adolescents (10–12 years). This study investigated the prevalence of STH infections, examined associated risk factors, and assessed their impact on the nutritional status of children and adolescents.

Methods

An analytical cross-sectional study was conducted within schools and took place from April to June 2023 and involved 382 participants in Calabar, Nigeria. All participants in the study completed a questionnaire designed to gather information on their demographics and knowledge, attitudes, and practices (KAP) regarding STH infections. Anthropometric measurements were taken according to World Health Organisation (WHO) standards. Fresh faecal samples were collected from each study participant and examined via the Kato-Katz technique. The data were analysed using STATA software, version 14. A binomial logistic regression model was used to identify predictors of STH infections and to examine the associations between STH infection status and stunting, underweight, and wasting.

Results

The overall prevalence of STHs was 28.8%, with Ascaris lumbricoides (19.6%) being the most prevalent. The prevalence of STHs was greater among males (30.2%) than females (27.7%) and was relatively greater among participants aged 10 years and above (34.8%). All study participants recorded light infection intensities. The prevalence rates of stunting, underweight, and wasting were 10.5%, 8.4%, and 6.3%, respectively. Respondents with no history of deworming were significantly less likely to contract an STH infection (Odds Ratio: 0.2; 95% Confidence Interval: 0.1–0.4; P < 0.001). The use of pit latrines was associated with a greater likelihood of STH infection (OR: 2.1; 95% CI: 1.3–3.4; P = 0.002). Additionally, respondents with poor attitude scores were significantly less likely to contract an STH infection (Adjusted Odds Ratio: 0.6; 95% CI: 0.4–0.8; P = 0.003), and those over 10 years old (OR: 0.1; 95% CI: 0.04–0.82; P = 0.027) were significantly less likely to be underweight than those aged 5–7 years. There was no association between stunting, underweight, wasting, and STH infection.

Conclusion

These findings highlight the necessity for an integrated approach to STH management and nutrition initiatives in Nigeria.

Background

Soil-transmitted helminth (STH) infections are the most widespread among neglected tropical diseases (NTDs), affecting approximately 1.5 billion individuals globally and thus representing the most prevalent infection worldwide [1]. In 2020, the World Health Organization (WHO) set ambitious goals to mitigate the impact of STH by aiming to eliminate it as a public health issue by 2030 [2]. While these infections can affect individuals of any age, preschool-aged and school-aged children (SAC) are particularly vulnerable [3]. In Africa, 42 countries are endemic for STH, with 284 million cases among both school-aged and preschool-aged children [4]. Persistent STH infections can lead to growth retardation, weight loss, anaemia, increased school absenteeism, and diminished academic performance [5]. In addition to their physical health impact, these infections can also impair cognitive development in children [6].

In Nigeria, STHs are prevalent and represent a significant public health issue [7] and various studies across the country have reported the prevalence of STH ranging from 13.2 to 80.9% [8]. Additionally, Imalele et al. [9] highlighted that soil-transmitted helminthiases continue to burden children, despite the implementation of an annual nationwide school-based mass drug administration (MDA) programme. Despite the substantial efforts made in Nigeria to control STH through regular school-based MDA, the persistence of these infections necessitates a thorough examination of the risk factors associated with infection and the overall morbidity burden.

In developing countries, malnutrition and STH infections frequently occur together, creating a combined health issue for children that impacts their overall well-being [10]. Soil-transmitted helminth infections can lead to malnutrition by depleting the host’s nutrients or impairing nutrient absorption [11]. According to the Nigeria Demographic and Health Survey (NDHS) 2008, 23% of children aged 6–59 months were underweight, 40.6% were stunted, and 13.9% were wasted. A decade later, the NDHS 2018 reported that 22% of children in the same age group were underweight, 37% were stunted, and 7% were wasted [12].

Despite research identifying factors linked to malnutrition in Nigerian children [13–15], there is a significant lack of data on how STH affects nutritional status. This is particularly relevant in the study area (Calabar), where there are no documented reports of similar studies among children and adolescents. Additionally, more studies are needed to evaluate the morbidity related to STH in children and adolescents to accurately assess the effectiveness of STH control programmes in the country. This study aimed to investigate the prevalence and risk factors of STH infections and the effect of STH infections on nutritional indices of children (5–9 years) and adolescents (10–12 years) in Calabar, Nigeria.

Methods

Study area

The study was carried out in Calabar, the capital of Cross River State, is a moderately populated city in Nigeria’s South‒South region, situated at longitude 8 19’30"E and latitude 4 57’0"N. The city experiences a tropical climate with an extended wet season and a short dry season, an average annual temperature of 28 °C, and approximately 3000 mm of annual precipitation [16]. Calabar includes both urban and peri-urban areas. Urban areas are distinguished by access to essential infrastructure, such as piped water, internet, healthcare, and educational facilities. Peri-urban areas, located on the city’s outskirts, lie between urban and rural zones and are primarily inhabited by low-income populations. These areas commonly feature substandard housing, unimproved latrines, and poor hygiene and environmental conditions.

Study design

A school-based analytical cross-sectional study was carried out from April to June 2023 among children (5–9 years) and adolescents (10–12 years) in four primary schools in Calabar. The schools were grouped into two categories based on the two local government areas (LGAs) in Calabar, with assistance from the state ministry of education. Two schools from each LGA were subsequently randomly selected (Fig. 1). Participants were selected through a systematic sampling technique from the four schools, using a roster as the sampling frame based on the total number of pupils enrolled during the 2022–2023 academic year. The sample size was proportionally distributed among the schools: 100 participants from Government Primary School Akim, 101 from Government Primary School Henshaw Town, 101 from Government Primary School Mayne Avenue, and 80 from Government Primary School Ikot Ansa (Fig. 1). The participants’ ages ranged from 5 to 12 years, and for analysis, the ages were categorized into three subgroups: 5–7 years, 8–10 years, and over 10 years, based on similar studies conducted by Genet et al. [17] and Imalele et al. [18].

Fig. 1.

Map of Calabar showing the specific sampling points. ArcMap version 10.8 was used to create the map

Sample size determination

The sample size for this study was estimated via the formula described by Bruno and Omar [19], 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 the 5% significance level and p = prevalence of soil-transmitted helminthiasis (46%) [18]. This calculation yielded a minimum sample size of 382.

Inclusion and exclusion criteria

The study targeted participants aged 5 to 12 years living in the designated districts. Only those whose parent gave consent for their children to participate were included in the study. The study included participants who provided complete samples and data. Potential participants were excluded if they were absent or unwell during the research period.

Ethical considerations

This study was carried out following the Helsinki Declaration, and approval was obtained from the Ethics and Research Committee of the Ministry of Health in Calabar, Cross River State, under REC number CRSMOH/HRP/REC/2023/416. School head teachers provided consent, and assent was obtained verbally from older school children before the study began. Additionally, the parents/legal guardians of the participating children granted permission on behalf of their children. Informed consent to participate was obtained from the parents/legal guardians of the study participants.

Data collection

Knowledge attitude and practice (KAP) questionnaire

All participants in the study completed a questionnaire in English designed to gather information on their demographics and knowledge, attitudes, and practices (KAP) regarding soil-transmitted helminth (STH) infections. This questionnaire was adopted from a study conducted by Mationg et al. [20]. This KAP questionnaire features both multiple-choice and open-ended questions covering demographic details, medical history, understanding of intestinal worms, modes of transmission, symptoms, and treatments for STH infections. It also assessed attitudes towards STH and self-reported hygiene behaviours such as hand washing, food handling, toilet use, and footwear habits. The questionnaire underwent a pretest at two different schools The questionnaire was pretested at two randomly selected schools from a Ministry of Education list to evaluate its clarity, relevance, and effectiveness. This allowed researchers to identify and resolve any issues, ensuring the questionnaire was suitable for the main study.

The questionnaire was administered by two trained health extension workers, with support from the class teachers. The first health extension worker read out the instructions and questions to the children in the classroom, whereas the second health extension worker and the class teacher moved around to ensure that all the pupils understood the instructions and answered the questions correctly.

Parasitological examination

Each study participant received a clean, labelled, leak-proof stool collection cup and was instructed to provide a morning stool sample about the size of a thumb the next day or, if necessary, the day after. Stool samples were collected from each school location and transported in a thermal box to the Department of Zoology and Environmental Biology laboratory at the University of Calabar, a nearby facility to the collection sites. Within two hours of collection, three Kato‒Katz thick smears from each sample were prepared onsite at the schools, and all smears were examined the same day [21]. For each sample, a spatula was used to transfer a portion of the stool onto tissue paper. A screen was then placed over the sample, allowing it to pass through the gauze and collect above it. The sieved material was scraped off with a spatula, and approximately 41.7 mg of each sample was transferred into a 6 mm hole on a 1.5 mm thick template on a microscope slide [22]. The template was carefully removed, leaving the sample on the slide. A pre-soaked cellophane strip was placed over the stool, and the slide was inverted and pressed firmly on a smooth, hard surface. The slide was then positioned with the cellophane side up to facilitate evaporation of water while glycerol cleared the faecal matter. The prepared Kato‒Katz slides were examined under a light microscope for the presence of STH eggs or larvae. Two trained laboratory scientist independently reviewed the slides. In cases where significantly different results were observed each slide were independently reviewed by a third qualified laboratory technician to confirm or refute the initial findings.

Finally, the results were documented on a laboratory report sheet. If at least one egg or larvae (for S. stercoralis) were seen on any of the three Kato-Katz thick smear slides, the participant was considered positive. The species-specific average egg count from the triplicate Kato-Katz slides was multiplied by 24 to evaluate the intensity of STH infection (A. lumbricoides, Hookworm, and T. trichiura) [23]. The number of eggs for each STH species was counted to determine the prevalence and intensity of infection (eggs per gram of faeces, EPG). The infection intensity for each species was classified as light, moderate, or heavy according to the WHO criteria [24].

Nutritional status assessment

At the start of the study, the height and weight of all the children included were measured. Height was recorded to the nearest 0.1 cm using a height scale chart (paper beam chart), and weight was measured to the nearest 0.1 kg with a digital weighing scale (SECA^® Hamburg, Germany). To identify malnutrition, the height-for-age Z score (HAZ) was used to determine stunting, the body mass index (BMI)-for-age Z score (BAZ) was used to assess wasting, and the weight-for-age Z score (WAZ) was used to evaluate underweight status. These Z scores were calculated via the SAS macros for the 2007 WHO Child Growth Standards for School-aged Children and Adolescents [25]. Children with Z scores below − 2 standard deviations (SDs) were classified as stunted (HAZ < -2 SDs), underweight (WAZ < -2 SDs), or wasted (BAZ < -2 SDs). The WHO 2007 growth chart uses the weight-for-age Z score only for children aged 5 to 10 years, as it is not suitable for growth monitoring beyond age 10. This limitation arises because it does not distinguish between height and body mass in older children [26]. For children under 10 years, underweight was assessed using the weight-for-age Z score. For those older than 10 years, BMI-for-age was evaluated in combination with height-for-age.

Study variables

The outcome variable was defined as the presence of at least one STH infection (Ascaris lumbricoides, Trichuris trichiura, hookworm, and/or Strongyloides stercoralis). Independent variables included age, gender, drinking water source, type of toilet facility, habit of wearing shoes, history of deworming, handwashing before and after eating, handwashing after using the toilet, washing fruits before and after eating, and knowledge, attitudes, and practices regarding STH prevention and control.

Data analysis

The data were initially entered into an Excel spreadsheet, cleaned, and then exported to STATA software, version 14 (StataCorp LLC Texas, USA), for analysis. Descriptive statistics were employed to summarize the sociodemographic characteristics of the study participants.

A t-test was used to compare the mean intensity of STH infections between males and females, whereas one-way ANOVA was used to assess differences in the arithmetic means of STH infections across various age groups. Descriptive statistics were employed to outline the sociodemographic traits of the participants, presenting frequencies and percentages for categorical data. To examine the relationships between independent variables and the outcome variable, the chi-square test was applied.

For the knowledge, attitude, and practice (KAP) questionnaire, each correct answer in the knowledge and attitude sections was assigned one point, incorrect answers received minus one point, and “do not know” responses were scored zero. In the practices section, “Never” responses were given a score of zero, “Some of the time” were given a score of one, and “Always” were given a score of two, reflecting the frequency of the behaviour.

The participants’ overall knowledge and practice scores were categorised as follows: scores of 20 or more indicated good knowledge/practice, scores between 11 and 19 indicated average knowledge/practice, and scores of 10 or less indicated poor knowledge/practice. Specifically, for knowledge of STH transmission and symptoms, scores of 5–6 were considered good, scores of 3–4 were considered average, and scores of 2 or less were considered poor. For STH prevention knowledge, scores of 7–9 were categorised as good, scores of 4–6 were categorised as average, and scores of 3 or less were categorised as poor.

Binomial logistic regression model was used to identify predictors of STH infections and to examine the associations between STH infection status and the likelihood of stunting, underweight, and wasting. The strength of these associations was expressed as odds ratios with 95% confidence intervals. A p-value of less than 0.05 was considered statistically significant.

Results

General characteristics of the study participants

A total of 382 participants were included in this study, with a majority being females (55.8%, n = 213). The mean age of the participants was 9.6 years (± 2.14 SD), with ages ranging from 5 to 12 years. The largest proportion of participants were in the 8–10 years age group (65.2%, n = 249) (Table 1). The mean weight and height of the study participants were 26.5 kg (± 5.34 SD) and 1.29 m (± 0.07 SD), respectively.

Table 1.

Sociodemographic characteristics of the study participants in Calabar (N = 382)

Characteristic	Number	Percentage
Gender
Male	169	44.2
Female	213	55.8
Age-group (Years)
5–7	41	10.7
8–10	249	65.2
> 10	92	24.1
School
Government Primary School Akim	100	21.2
Government Primary School Henshaw Town	101	26.4
Government Primary School Mayne Avenue	101	26.4
Government Primary School Ikot Ansa	80	20.9
Mother’s Occupation
Trader	112	29.3
Civil servant	144	37.7
Unemployed	40	10.5
Others	86	22.5
Father’s Occupation
Trader	136	35.6
Civil servant	122	31.9
Unemployed	27	7.1
Others	97	25.4

Prevalence and intensity of STH and nutritional characteristics of the study participants

The overall prevalence of STHs was 28.8% (n = 110) [95% CI 24.2–33.3%], with Ascaris lumbricoides being the most identified parasite, which was found in 19.6% (n = 75) [95% CI 15.6–23.6%] of the study participants. Trichuris trichiura, hookworm, and larvae of Strongyloides stercoralis were detected in 5.2% (n = 20) [95% CI 3.0-7.5%], 2.9% (n = 11) [95% CI 1.2–4.6%], and 2.6% (n = 10) [95% CI 1.0-4.2%] of the participants, respectively. The prevalence of STHs was greater among males (30.2%, n = 51) [95% CI 25.6–34.8%] than females (27.7%, n = 59) [95% CI 22.0-33.5%] (P = 0.595). Additionally, the prevalence was relatively greater among participants aged 10 years and above (34.8%, n = 32) [95% CI 25.1–44.5%] than among those aged 5–7 years (29.3%, n = 12) [95% CI 15.3–43.2%] and those aged 8–10 years (26.5%, n = 66) [95% CI 21.0–32.0%] (P = 0.325) (Fig. 2).

Fig. 2.

Prevalence of STH among study participants in Calabar

Overall, A. lumbricoides presented the highest infection intensity (6.785 ± 0.794 eggs per gram, EPG), followed by T. trichiura (1.947 ± 0.358 EPG) and hookworm (1.319 ± 0.331 EPG). The intensities of T. trichiura (2.478 ± 0.550 EPG) and hookworm (1.464 ± 0.454 EPG) infections were greater in females, whereas A. lumbricoides infection (7.952 ± 1.316 EPG) was more intense in males. However, no significant sex-related differences in infection intensity were observed (p > 0.05) (Fig. 3).

Fig. 3.

Mean intensity of STH infection among study participants in Calabar

Across different age groups, the intensity of STH infections did not significantly differ (p > 0.05) among the study participants. The intensities of A. lumbricoides (9.130 ± 1.733 EPG) and T. trichiura (2.086 ± 0.881 EPG) infections were greater in participants older than 10 years, whereas hookworm (1.756 ± 1.295 EPG) infections were more common in those aged 5–7 years (Fig. 3). Overall, all study participants recorded light infection intensities.

The prevalence rates of stunting, underweight and wasting were 10.5% (40/382), 8.4% (32/382 and 6.3% (24/382), respectively.

Knowledge of STH

The study revealed that 70.2% of the respondents were aware of STHs. With respect to the method of STH transmission, 50.3% of the respondents incorrectly identified mosquito bites as a transmission route. Others reported contaminated food (42.9%), while additional behaviours cited included playing in contaminated areas (34.6%), playing with soil (31.7%), and walking barefoot (15.1%). Contact with infected faeces (11.5%) and playing in untidy environments (17.8%) were less common transmission methods. Only 16.8% of the respondents demonstrated a strong understanding of STH transmission, while the majority displayed either moderate (41.4%) or poor (41.9%) knowledge.

Fever and stomach ache were recognized by 46.6% and 43.7% of the respondents, respectively, as signs and symptoms of STH infection. Other frequently identified symptoms included diarrhoea (37.7%), low blood pressure (31.2%), and being overweight (26.7%). Less commonly recognized symptoms included weight loss (20.4%), loss of appetite (18.3%), blood loss (17%), growth impairment (13.5%), and nausea (10.2%). Overall, a small proportion of respondents (4.97%) exhibited strong knowledge of the signs and symptoms of STH. The majority possessed moderate knowledge (35.08%), whereas a significant portion (59.95%) had poor knowledge.

The preventive measures most widely recognized included washing fruits before consumption (76.7%) and washing hands before eating (75.1%). Washing hands after using the toilet was reported by 68.1% of the respondents. Less commonly recognized preventive measures included the use of mosquito nets (33.3%), proper toilet facilities (25.1%), and regular exercise (28.5%). Some respondents incorrectly identified excessive food consumption (12.3%) as a preventive measure. Overall, only 13.6% of the respondents demonstrated good knowledge of STH prevention, whereas nearly half (49.5%) had moderate knowledge, and 36.9% had poor knowledge.

In terms of overall knowledge of STH, only 11.3% of the respondents possessed a strong understanding. Most of the participants had moderate overall knowledge (62.0%), whereas 26.7% had poor overall knowledge. A total of 86 respondents (22.5%) exhibited good attitudes, whereas 106 (27.8%) displayed poor attitudes toward STHs. Finally, 87 respondents (22.8%) reported good practice scores, whereas 191 (50.0%) reported average practice scores related to STH infections (Table 2).

Table 2.

Knowledge of STH transmission, signs and symptoms and prevention among study participants in Calabar (N = 382)

Variables	Number	Percentage
Heard about STH
Yes	268	70.2
No	114	29.8
STH Transmission
Walk barefoot	58	15.1
Eating contaminated food	164	42.9
Eating undercooked and unwashed vegetables	60	15.7
Contact with faeces of an infected person	44	11.5
Mosquito bite	192	50.3
Playing in contaminated areas	132	34.6
Playing with soil	121	31.7
Playing in dirty places	68	17.8
Overall STH transmission knowledge
Good	64	16.8
Average	158	41.4
Poor	160	41.9
Knowledge about STH signs and symptoms
Weight loss	78	20.4
Stomach ache	167	43.7
Diarrhoea	144	37.7
Growth impairment	51	13.5
Nausea	39	10.2
Loss of appetite	70	18.3
Blood loss	65	17.0
Fever	178	46.6
Overweight	102	26.7
Low blood pressure	119	31.2
Overall knowledge about signs and symptoms
Good	19	4.97
Average	134	35.08
Poor	229	59.95
Knowledge about STH prevention
Eating too much food	47	12.3
Using mosquito net	127	33.3
Using the toilet	96	25.1
Washing fruits before eating	293	76.7
Washing your hands before eating	287	75.1
Washing your hands after using the toilet	260	68.1
Regular exercise	109	28.5
Overall knowledge about STH prevention
Good	52	13.6
Average	189	49.5
Poor	141	36.9
Overall knowledge score
Good	43	11.3
Average	237	62.0
Poor	102	26.7
Overall attitude score
Good	86	22.5
Average	190	49.7
Poor	106	27.75
Overall practice score
Good	87	22.8
Average	191	50.0
Poor	104	27.2

Water access, sanitation practices, and perceptions of STH prevention among respondents

Approximately 93% of the respondents had access to potable water, whether bottled water or a hand pump. Most participants utilized pit latrines (47.6%), closely followed by those who used a water closet system (46.1%). However, 6.3% of the respondents still engaged in open defecation. Approximately 58% of the study participants reported having previously received deworming medication, whereas 41.6% had never taken such drugs. With respect to hand hygiene after using the toilet, 34.3% of the respondents always washed their hands, 37.9% sometimes did, and 27.8% never did. When asked about washing their hands before and after meals, 39.9% of the respondents stated that they always do, 35.9% sometimes do, and 26.2% never do. Similarly, 42.7% of the respondents always washed their fruits and vegetables before eating, whereas 33.8% sometimes did, and 23.6% never did. For the practice of walking barefoot, 34.0% of the respondents reported doing so always, 40.9% sometimes, and 25.1% never walked barefoot. Most respondents (63.6%) do not perceive STH as a serious disease, whereas 89.0% believe that STH can be prevented (Table 3).

Table 3.

Factors associated with STH infection among study participants in Calabar (n = 382)

Variables	Frequency (%)	STH		OR (95% CI)	P value	AOR (95% CI)	P value
		Positive, n (%)	Negative, n (%)
Gender
Male	169 (44.2)	51 (30.2)	118 (69.8)	Reference
Female	213 (55.8)	59 (27.7)	154 (72.3)	0.9 (0.6–1.4)	0.595	0.7 (0.4–1.2)	0.329
Source of Drinking Water
Potable water/bottled water/hand pump	356 (93.2)	106 (29.8)	250 (70.2)	Reference
Unprotected well/Reservoir	26 (6.8)	4 (15.4)	22 (84.6)	0.4 (0.1–1.3)	0.097	0.4 (0.1–1.4)	0.182
Type of Toilet
Water Closet	176 (46.1)	38 (21.6)	138 (78.4)	Reference
Pit Toilet	182 (47.6)	67 (36.8)	115 (63.2)	2.1 (1.3–3.4)	0.002	1.0 (0.5–1.8)	0.942
Open defecation	24 (6.3)	5 (20.8)	19 (79.2)	1.9 (0.3–2.7)	0.932	0.9 (0.2–2.7)	0.862
Received worm medicine before
Yes	223 (58.4)	87 (39.0)	136 (60.9)	Reference
No	159 (41.6)	23 (14.5)	136 (85.5)	0.2 (0.1–0.4)	< 0.001	0.2 (0.1–0.5)	< 0.001
Washing hands after using the toilet
Always	131 (34.3)	37 (28.2)	94 (71.8)	Reference
Sometimes	145 (37.9)	40 (27.6)	105 (72.4)	0.9 (0.5–1.6)	0.903	0.9 (0.5–1.7)	0.941
Never	106 (27.8)	33 (31.1)	73 (68.8)	1.1 (0.6-2.0)	0.628	1.1 (0.6–2.1)	0.615
Washing hands before and after eating
Always	145 (37.9)	45 (31.0)	100 (68.9)	Reference
Sometimes	137 (35.9)	43 (31.4)	94 (68.6)	1.0 (0.6–1.6)	0.949	1.0 (0.6–1.8)	0.852
Never	100 (26.2)	22 (22.0)	78 (78.0)	0.6 (0.3–1.1)	0.120	0.5 (0.3–1.1)	0.103
Washing fruits and vegetables before eating
Always	163 (42.7)	45 (27.6)	118 (72.4)	Reference
Sometimes	129 (33.8)	33 (25.6)	96 (74.4)	0.9 (0.5–1.5)	0.698	0.9 (0.5–1.7)	0.984
Never	90 (23.6)	32 (35.6)	58 (64.4)	1.4 (0.8–2.5)	0.189	1.4 (0.8–2.6)	0.208
Walking barefooted
Always	130 (34.0)	40 (30.8)	90 (69.2)	Reference
Sometimes	156 (40.9)	44 (28.2)	112 (71.8)	0.8 (0.5–1.4)	0.636	0.8 (0.4–1.4)	0.465
Never	96 (25.1)	26 (27.1)	70 (72.9)	0.8 (0.4–1.4)	0.547	0.9 (0.4–1.7)	0.785
Believe STH is a serious disease
Yes	139 (36.4)	46 (33.1)	93 (66.9)	Reference
No	243 (63.6)	64 (26.3)	179 (73.7)	0.7 (0.4–1.1)	0.161	0.7 (0.4–1.1)	0.212
Believe STH can be prevented
Yes	340 (89.0)	96 (28.2)	244 (71.8)	Reference
No	42 (10.9)	14 (33.3)	28 (66.7)	1.2 (0.6–2.5)	0.492	1.0 (0.4–2.1)	0.954

Additionally, an analysis of sanitation and hygiene practices by age group was conducted, with a focus on handwashing habits, toilet use, and walking barefoot. The results revealed slight variations in hygiene and sanitation practices across age groups, though not statistically significant. Among children, 46.3% aged 5–7 years and 49.8% aged 8–10 years used pit toilets, compared to 42.4% of adolescents older than 10 years. Furthermore, open defecation was reported among 2.4% and 7.6% of children aged 5–7 years and 8–10 years, respectively, as well as among 4.4% of adolescents aged over 10 years (P = 0.292). After using the toilets, 39.0% of children aged 5–7 years, 35.3% of those aged 8–10 years, and 29.4% of adolescents (> 10 years) always washed their hands. In contrast, 17.1% of children aged 5–7 years, 30.9% of those aged 8–10 years, and 23.9% of adolescents (> 10 years) never washed their hands (P = 0.112). Handwashing before and after meals was practiced by 29.3% of children aged 5–7 years, 39.8% of children aged 8–10 years, and 37.0% of adolescents (aged > 10 years). In contrast, 34.2% of children aged 5–7 years, 26.9% of those aged 8–10 years, and 20.7% of adolescents never engaged in this practice (P = 0.318). Also, 34.2% of children aged 5–7 years, 34.1% of children aged 8–10 years, and 33.7% of adolescents (> 10 years) always walked barefoot. In contrast, 24.4% of children aged 5–7 years, 27.3% of those aged 8–10 years, and 19.6% of adolescents (> 10 years) reported never walking barefoot (P = 0.605).

Factors associated with STH infection

Interestingly, univariate logistic regression analysis revealed that respondents with no history of taking deworming medication were significantly less likely to contract an STH infection (OR: 0.2; 95% CI: 0.1–0.4; P < 0.001). This finding was further corroborated by multivariate analysis, which yielded similar results (AOR: 0.2; 95% CI: 0.1–0.5; P < 0.001). Additionally, the use of pit latrines was associated with a greater likelihood of STH infection (OR: 2.1; 95% CI: 1.3–3.4; P = 0.002). Although not statistically significant, females (OR: 0.9; 95% CI: 0.6–1.4; P = 0.595) and those who used unprotected wells or reservoirs (OR: 0.4; 95% CI: 0.1–1.3; P = 0.097) were also less likely to have an STH infection. The other variables examined were not significantly associated with STH infection (Table 3).

The respondents with average overall knowledge of STH transmission (OR: 1.1; 95% CI: 0.6–1.9; P = 0.15) were more likely to be infected with STH. Similarly, those with poor overall knowledge scores (OR: 1.1; 95% CI: 0.5–2.4; P = 0.855) also presented a greater likelihood of STH infection. With respect to overall practice scores, respondents with both average (OR: 1.1; 95% CI: 0.6-2.0; P = 0.621) and poor scores (OR: 1.1; 95% CI: 0.6–2.2; P = 0.607) demonstrated similar odds of being infected with STH. Interestingly, respondents with poor attitude scores were significantly less likely to contract an STH infection (OR: 0.4; 95% CI: 0.1–0.6; P = 0.002). This finding was further corroborated by multivariate analysis, which yielded similar results (AOR: 0.6; 95% CI: 0.4–0.8; P = 0.003) (Table 4).

Table 4.

Association between knowledge, attitudes and practice scores and STH infection among study participants in Calabar

Characteristic	Category	STH		OR (95% CI)	P value	AOR (95% CI)	P value
		Positive, n (%)	Negative, n (%)
Overall knowledge of STH Transmission score	Good	18 (28.1)	46 (71.9)	Reference
	Average	46 (29.1)	112 (70.9)	1.1 (0.6–1.9)	0.150	0.9 (0.8-1.0)	0.524
	Poor	46 (28.8)	111 (71.3)	1.0 (0.5–1.9)	0.090	1.3 (0.8-2.0)	0.306
Overall knowledge score	Good	12 (27.9)	31 (72.1)	Reference
	Average	68 (28.7)	169 (71.3)	1.0 (0.5–2.1)	0.917	0.9 (0.6–1.3)	0.701
	Poor	30 (29.4)	72 (70.6)	1.1 (0.5–2.4)	0.855	0.9 (0.6–1.5)	0.858
Overall attitude score	Good	33 (38.4)	53 (61.6)	Reference
	Average	58 (30.5)	132 (69.5)	0.7 (0.4–1.2)	0.200	1.9 (0.8–4.4)	0.113
	Poor	19 (17.9)	87 (82.1)	0.4 (0.1–0.6)	0.002	0.6 (0.4–0.8)	0.003
Overall practice score	Good	23 (26.4)	64 (73.6)	Reference
	Average	56 (29.3)	135 (70.7)	1.1 (0.6-2.0)	0.621	1.0 (0.7–1.4)	0.700
	Poor	31 (29.8)	73 (70.2)	1.1 (0.6–2.2)	0.607	1.1 (0.7–1.4)	0.440

Associations between STH infection and nutritional indicators

The prevalence of stunting (11.3%), underweight (9.4%), and wasting (6.6%) was greater among females than among males; however, this difference was not statistically significant (P > 0.05). Stunting (17.1%) and underweight (14.6%) were more prevalent among participants aged 5–7 years, whereas wasting (7.6%) was more common in those over 10 years old (P > 0.05) (Table 5).

Table 5.

Associations between the prevalence of STH and nutritional indices among study participants in Calabar

Variable	Total (N)	Stunting n (%)	Univariate OR (95% CI)	P Value	Underweight n (%)	Univariate OR (95% CI)	P Value	Wasting (%)	Univariate OR (95% CI)	P Value
Gender
Male	169	16 (9.5)	Reference		12 (7.1)	Reference		10 (5.9)	Reference
Female	213	24 (11.3)	1.2 (0.6–2.3)	0.569	20 (9.4)	1.3 (0.6–2.8)	0.424	14 (6.6)	1.1 (0.4–2.5)	0.793
Age-Group
5–7	41	7 (17.1)	Reference		6 (14.6)	Reference		2 (4.9)	Reference
8–10	249	27 (10.8)	0.5 (0.2–1.4)	0.255	23 (9.2)	0.5 (0.2–1.5)	0.290	15 (6.0)	1.2 (0.2–5.6)	0.773
> 10	92	6 (6.5)	0.3 (0.1-1.0)	0.068	3 (3.3)	0.1 (0.04–0.82)	0.027	7 (7.6)	1.6 (0.3-8.0)	0.566
Any STH
Positive	110	10 (9.1)	0.8 (0.3–1.7)	0.576	7 (6.4)	0.6 (0.2–1.6)	0.369	9 (8.2)	1.5 (0.6–3.6)	0.334
Negative	272	30 (11.0)	Reference		25 (9.2)	Reference		15 (5.5)	Reference

According to the univariate logistic regression analysis, the odds of stunting (OR: 1.2; 95% CI: 0.6–2.3; P = 0.569), underweight (OR: 1.3; 95% CI: 0.6–2.8; P = 0.424) and wasting (OR: 1.1; 95% CI: 0.4–2.5; P = 0.793) were greater in females than in males. Participants aged 8–10 years (OR: 0.5; 95% CI: 0.2–1.4; P = 0.255) and those over 10 years (OR: 0.3; 95% CI: 0.1-1.0; P = 0.068) were less likely to be stunted than those aged 5–7 years. Moreover, participants over 10 years old (OR: 0.1; 95% CI: 0.04–0.82; P = 0.027) were significantly less likely to be underweight than those aged 5–7 years. However, the odds of being wasted were greater among participants aged 8–10 years (OR: 1.2; 95% CI: 0.2–5.6; P = 0.773) and those over 10 years (OR: 1.6; 95% CI: 0.3-8.0; P = 0.566) than among those aged 5–7 years (Table 5).

There was no significant association between stunting, underweight, wasting, and STH infection. Interestingly, the odds of being stunted (OR: 0.8; 95% CI: 0.3–1.7; P = 0.576) and underweight (OR: 0.6; 95% CI: 0.2–1.6; P = 0.369) were lower in STH-positive individuals than in STH-negative individuals. Conversely, the odds of wasting were greater (OR: 1.5; 95% CI: 0.6–3.6; P = 0.334) among STH-positive individuals than among their negative counterparts (Table 5).

Discussion

Soil-transmitted helminth (STH) infections remain a major public health issue in developing countries, especially impacting children, who are more susceptible to these infections [3]. The aim of this study was to assess the prevalence of STH infections, identify related risk factors, and evaluate their effects on the nutritional status of school-aged children. Despite ongoing MDA programmes in the study area, a significant number of children are still affected by STH infections. Additionally, instances of stunting, undernutrition, and wasting were identified among participants. Misunderstandings about STH transmission, symptoms, and prevention were widespread, highlighting the need for enhanced educational programmes and interventions to improve awareness and understanding of STH transmission.

Findings from this study revealed an overall STH prevalence of 28.8% among participants in Calabar, Cross River State, surpassing the WHO’s morbidity control target of less than 20%. The data indicate that STH infections persist as a significant public health concern in the study area, a trend similar to that reported by Imalele et al. [9] and Usang et al. [27]. The most common species was A. lumbricoides (19.6%), followed by T. trichiura (5.2%), with lower rates of hookworm (2.9%) and S. stercoralis (2.6%). These findings align with previous observations by Usang et al. [27]. Other studies across Nigeria have reported higher prevalence rates of A. lumbricoides among children than other STHs [7, 8, 28]. The relatively elevated prevalence of A. lumbricoides noted in this study could be attributed to the resilience of its eggs under diverse environmental conditions, their high fecundity, and the adhesive properties of their shells, which facilitate attachment to human hands, fruits, and vegetables [29].

The KAP survey indicated that 70.2% of the participants reported being familiar with STHs; however, further questioning revealed gaps in knowledge in several areas. There was notable poor knowledge about the modes of STH transmission, the symptoms of infection, and preventive strategies. This points to a deficiency in health education regarding STH among the respondents. Most participants exhibited either moderate or inadequate knowledge of STH transmission, as well as attitudes and practices related to infection. A poor understanding of STH transmission may result in ineffective preventive measures, thereby increasing the risk of infection. This concern is substantiated by the fact that 50% of the respondents demonstrated moderate attitudes and 27.2% displayed poor attitudes towards STH infection. This highlights the necessity for enhanced educational initiatives and interventions to increase awareness and comprehension of STH transmission, which could foster better attitudes and subsequently reduce the prevalence and spread of these infections.

Also, findings indicate that the majority of children across all age groups use pit toilets, reflecting some level of access to basic sanitation facilities. However, the higher prevalence of open defecation among participants aged 8–10 years (7.6%) compared to participants aged 5–7 years (2.4%) and those > 10 years (4.4%) suggests potential gaps in sanitation education or accessibility for this age group. Although the differences are not statistically significant (P = 0.292), they highlight the need for targeted interventions, particularly for school-age children, to improve sanitation practices and reduce the risk of soil-transmitted helminth infections. This could include hygiene education and ensuring consistent access to appropriate toilet facilities.

The study revealed that 6.3% of participants continued to practice open defecation, whereas the use of pit latrines was linked to a significantly greater risk of STH infections (OR: 2.1; 95% CI: 1.3–3.4; P = 0.002). According to Genet et al. [17], traditional pit latrines are inadequate for preventing STH infections, as they do not fully contain faecal pathogens, which can lead to contamination. Furthermore, the open nature of these latrines provides a suitable breeding ground for flies, which can spread these pathogens to surrounding areas, increasing the risk of transmission and infection. Similar findings were reported by Baker and Ensink [30] in Tanzania. Furthermore, both open defecation and the use of pit latrines have been strongly associated with STH infections [18, 31, 32]. Environmental contamination with STH ova, largely due to open defecation, results in children contaminating their hands when playing with soil [33]. This elevates the risk of ingesting the ova through direct hand-to-mouth contact or by handling food with unwashed hands, increasing the likelihood of STH infection. Notably, 37.9% of the participants washed their hands occasionally, whereas 27.8% never did.

Approximately 58% of the study participants reported having previously received deworming medication, whereas 41.6% had never taken such drugs. Interestingly, the study revealed that respondents with no history of taking deworming medication were significantly less likely to contract an STH infection. This result may suggest that individuals who have not taken deworming medication may engage in other preventive behaviours that reduce their risk of infection. This is seen in the respondents’ responses to questions on personal hygiene, although there was no significant variation from those with poor personal hygiene practices. This unexpected result may also indicate potential issues with the regular use of deworming medication, such as improper use, overreliance on medication without accompanying hygiene practices, or the possibility of drug resistance. These findings emphasize the importance of integrating deworming programmes with comprehensive public health strategies that include education on hygiene and sanitation to effectively prevent STH infections.

Surprisingly, individuals with lower attitude scores were significantly less likely to acquire an STH infection (OR: 0.4; 95% CI: 0.1–0.6; P = 0.002). This outcome was further supported by multivariate analysis, which produced comparable results (AOR: 0.6; 95% CI: 0.4–0.8; P = 0.003). The consistency of this result across both univariate and multivariate analyses reinforces the validity of the observation, indicating that the association is unlikely to be caused by confounding variables. This also underscores the complexity of the link between health attitudes and actual health outcomes, suggesting that further research is needed to clarify which behaviours are associated with a “poor attitude” and how they might affect STH transmission.

Although most participants in the study reported having access to improved drinking water sources, the prevalence of STH infections remained elevated. Since data on household sanitation levels were not gathered in this study, these unmeasured factors may contribute to STH transmission. However, the low prevalence of hookworm and S. stercoralis infections observed may indicate limited faecal contamination in the environment, resulting in a reduced infection risk for these parasites in the study area. No associations were found between STH infections and variables such as sex, gender, water source, handwashing after toilet use, handwashing before and after meals, washing fruits and vegetables before consumption, walking barefoot, or overall knowledge and practices regarding STH among school-aged children, which differs from the findings of previous studies [34–37]. Nonetheless, risk factors for STH infections can vary across locations depending on the geography, environmental sanitation, lifestyle, and cultural practices of the local population [38].

The observed rates of stunting (10.5%), underweight (8.4%), and wasting (6.3%) in this study were lower than those reported in earlier studies conducted in Nigeria [15, 39, 40] and other countries [41, 42]. Despite these lower prevalence figures, they continue to be classified as public health concerns under the WHO standards [43].

In our study, female children were observed to have higher rates of stunting, underweight, and wasting than their male counterparts. This may be explained by gender-based disparities in nutrition and healthcare access may disproportionately impact females. For example, girls might receive less access to nutritious food or medical services than boys do, increasing their susceptibility to malnutrition-related conditions such as stunting, wasting, and underweight [44]. These findings align with the studies of Mahmood et al. [45], and Yisak et al. [46], which were conducted in Ethiopia, and Pakistan, respectively, but contrast with the reports of Chowdhury et al. [47], Poda et al. [48], and Hailegebriel [49].

Children between the ages of 8 and 10 years presented a lower likelihood of stunting than those between 5 and 7 years. This contrasts with findings from previous studies [50, 51]. Younger children, particularly those in the 5–7 years of age range, tend to be more susceptible to adverse environmental influences such as food scarcity, inadequate sanitation, and limited access to health care. These factors can significantly hinder their growth and development, resulting in elevated stunting rates compared with those of older children, who may have outgrown their most critical years of vulnerability [52]. Furthermore, individuals above the age of 10 years presented a notably lower likelihood of being classified as underweight than did those between the ages of 5 and 7 years. These findings align with the studies conducted by Degarege et al. [53] and Erismann et al. [54] in Ethiopia and Burkina Faso, respectively. As children mature, they may gain improved access to a more diverse range of foods or acquire healthier eating practices, thereby enhancing their nutritional status compared to younger children, who may still be dependent on caregivers for their meals [53].

Nevertheless, the likelihood of experiencing wasting was greater among participants aged 8–10 years and those older than 10 years than among those aged 5–7 years. This observation aligns with the findings of Herrador et al. [55] and Getaneh et al. [56] in Ethiopia. A plausible explanation for this trend is that, as children grow older, household socioeconomic conditions may shift, interacting with behavioural and biological factors that significantly contribute to the risk. As noted by Getaneh et al. [56], wasting was more prevalent among school-aged children from lower socioeconomic backgrounds than among those from wealthier families.

No statistically significant correlation was detected between stunting, underweight, and wasting and STH infection. Notably, the likelihood of being stunted and underweight was lower in individuals who tested positive for STH than in those who were negative. In contrast, the likelihood of wasting was elevated in STH-positive individuals relative to their negative counterparts. These findings align with the results of Degarege et al. [53]. The impact of helminth infections on a host’s nutritional status is more severe when infections are prolonged and intense [57]. All the STH infections reported in this study were of low intensity.

Limitations

Recall biases may be present among participants responding to inquiries about past events. Additionally, the cross-sectional design utilized in this study poses a limitation, as it precludes the evaluation of causal relationships between STH and the identified risk factors. Furthermore, the study did not measure micronutrient intake or red blood cell counts in the children. Moreover, factors like the presence of other parasites such as Plasmodium, participants’ dietary needs, and socio-economic status can greatly impact the nutritional indices observed. Therefore, future research of a similar nature should address these limitations.

Conclusion

This study revealed the widespread occurrence of STH, stunting, undernutrition, and wasting among school-aged children in the study population, although no association was found between STH infection and nutritional status of participants. These findings however highlight the necessity for an integrated approach to STH management and nutrition initiatives in Nigeria. Continuous deworming, coupled with targeted health education for both parents and children, enhancements in sanitation infrastructure, the promotion of better hygiene practices, and a long-term nutrition strategy, could offer the comprehensive control measures needed to enhance the health and overall welfare of school-aged children.

Author contributions

U.A.U. and I.E.E. contributed to concept, design, analysis and interpretation of the data, drafting and revision of the manuscript, and administrative/technical support. I.E.E. and E.E.O. contributed to the design, analysis and interpretation of the data, drafting and revision of the manuscript, and administrative / technical support. E.I.E. contributed to analysis and interpretation of the data, critical revision of the manuscript, and supervision. U.U.K. contributed to concept, design, acquisition and interpretation of data, drafting and revision of manuscript and supervision. All authors have read and approved the final manuscript.

Funding

The authors received no funding for this study.

Data availability

All data generated or analysed during this study are included in this published article.

Declarations

Ethics approval and consent to participate

This study was carried out following the Helsinki Declaration, and approval was obtained from the Ethics and Research Committee of the Ministry of Health in Calabar, Cross River State, under REC number CRSMOH/HRP/REC/2023/416. School head teachers provided consent, and assent was obtained verbally from older school children before the study began. Additionally, the parents/legal guardians of the participating children granted permission on behalf of their children. Informed consent to participate was obtained from the parents/legal guardians of the study participants.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.