Relationship between soil transmitted helminths, nutritional status and cognitive function among school children in Lusaka district, Zambia

Abstract

Soil Transmitted Helminths (STHs) are among the Neglected Tropical Diseases and are responsible for helminth infections worldwide, particularly in school aged children. This study was aimed at investigating the association of STHs with nutritional status and cognitive impairment among school children. A single stool sample was collected from each child from March to September 2022 from three public and one community schools in Lusaka District. The 209 total collected samples were processed using the Kato Katz method. Body Mass Index (BMI) was used to determine nutritional status. The working memory and processing speed were used to assess cognitive function. Of the 209 collected samples, 10 (4.8%; 95%CI: 2.3–8.6) were positive for STHs. Ascaris lumbricoides and hookworm were common parasites identified; Taenia spp, Schistosoma mansoni and Strongyloides stercolaris were also identified, all with light infections. The prevalence of STHs was significantly higher in males (9.7%; 7/72) compared to females (2.2%; 3/137) (p = 0.021). Younger children (8–12 years) had a higher prevalence (p = 0.022). Soil Transmitted Helminth infection had no influence on working memory and processing speed (p = 0.604) and on Mathematics and English scores attained by the children. Infection status was also not associated with nutritional status. STHs are prevalent in children. Further large-scale studies are required to establish whether infection status has significant influence on BMI and cognitive function.

Introduction

Soil Transmitted Helminths (STHs) are among the Neglected Tropical Diseases (NTDs) which infect people worldwide, especially in poverty settings. The STHs infections are caused by parasitic nematodes including Ascaris lumbricoides, Trichuris trichiura and hookworm (Ancylostoma duodenale and Necator americanus) (Pabalan et al. 2018) which are widely distributed in tropical and subtropical areas. It is reported that more than 1 billion people have STHs infections, with the greatest burden on children (WHO 2012). The parasites are transmitted to humans by eggs that are passed in the faeces of infected people through egg ingestion (Ascaris lumbricoides, Trichuris trichiura) or larval skin penetration (hookworm). Adult worms live in the intestines where they produce thousands of eggs each day. When the eggs are excreted, one of the following may occur; (i) ingesting eggs that are attached to vegetables when the vegetables are not carefully cooked, washed or peeled; (ii) ingesting eggs from contaminated water sources; (iii) children ingesting eggs when they play in contaminated soil and then put their hands in their mouths without washing them, and (iv) active penetration of hookworm larvae into the skin when people walk barefoot on the contaminated soil. Because excreted eggs need about three weeks to mature in the soil before they become infective, there is no direct person-to-person transmission, or infection from fresh faeces (WHO 2023). Infection intensity varies, people with light intensity STHs infections can be asymptomatic, but high infections can cause anaemia, diarrhoea, abdominal pain, malnutrition, impaired growth and delayed development, among other symptoms (WHO 2012). In addition, intestinal obstruction can be caused by infections of very high intensity.

Helminth infections tend to show severe health outcomes in children, with the infected eventually developing chronic disease conditions, including multi-organ damage, malnutrition, micronutrient deficiencies, stunted growth and impaired cognitive development, as well as reduced physical fitness (Bethony et al. 2006; Pullan et al. 2014). Over 260 million preschool-age children, 654 million school-age children, 108 million adolescent girls and 138.8 million pregnant and lactating women live in areas where STHs parasites are intensively transmitted particularly in low to middle-income countries. These are in need of treatment and preventive interventions (Sartorius et al. 2021). One geospatial analysis study conducted in 2020 which included surveys of STHs in children in sub-Saharan Africa conducted between 2000 and 2018, showed a prevalence of 13% (Sartorius et al. 2021), a significant drop from 44% seen in the year 2000. With the World Health Organization 2021–2030 Neglected Tropical Diseases Roadmap and goal of reducing the proportion of moderate and high intensity infections to less than 2% in 70% and 96% of endemic countries by 2025 and 2030, respectively (WHO 2020), it is hoped that the prevalence of STHs will continue to drop.

In Zambia, prevalence surveys on helminths conducted in Kafue, Siavonga and Mazabuka districts between 2010 and 2017 among pre-school children indicated that soil-transmitted helminths were common (Siwila et al. 2010; Halwindi et al. 2017) despite the Ministry of Health led bi-annual deworming programmes. A study in Chililabombwe district in 2017 further highlighted occurrence of STHs infections (Tembo et al. 2019). On the other hand, a study conducted in Kanyama, Madimba, Chaisa and George Compounds of Lusaka District, established that helminths ova particularly A. lumbricoides were also highly prevalent (> 60%) in pit latrines, indicating the presence of these parasites in humans using the latrines (Mbewe 2020). Despite these studies, there is limited information on whether there is a relationship between STHs and cognitive impairment among Zambian school aged children. This study was therefore aimed at investigating the association between STHs and cognitive impairment, and STHs and nutritional status among school children.

Materials and methods

Study design and area

This was a cross-sectional study conducted from March to September 2022. The study was conducted in Kaunda Square Township of Lusaka, the capital city of Zambia. Kaunda Square is a township which is approximately 1.26 km² in size with a population of approximately 34 882 (CSO 2010). Inhabitants of the township depend on both formal and informal/self-employment (street vending, carpentry, tailoring, block-making, charcoal trading, retail trading and other business ventures) (Twambo and Kabubi 2018). The township has three secondary, three public primary and two community schools. In this study, children in the three primary and one community schools were randomly selected and included. The research targeted Tunduya, Kaunda Square and Mumana primary schools and Mango Grove Community School. School children aged 8–16 years were included in the study.

Sampling

Multistage sampling was used. In the schools, the grades 2–9 were selected. Thereafter, one class was randomly selected from each of the grades. Finally, 15 children were randomly selected from each class (on average, a class had approximately 35–50 learners). This was achieved by writing numbers on pieces of paper, placing them in a plastic bag, mixing and picking one paper at a time. Stool was then collected from each child using a small mouthed, tight and leak proof container with aid of a spatula. A health worker from the local health facility assisted with the sample collection.

Parasitological analysis of samples

During sample collection, the stool containers were labelled with the participant’s identification code, sex, age, date and time of collection. The specimens were transported in cool boxes packed with ice within 30 min of collection to the University of Zambia, School of Veterinary Medicine Parasitology laboratory. The stool samples were analysed under a microscope following preparation using the Kato-Katz technique (WHO 2019). For each sample, duplicate slides were prepared and read by the researcher and a qualified technician. Slides were read twice; first within 30–60 min for detection of hookworm eggs and again within 2 h for detection of the other parasites. Egg per gram of faeces (EPG) was used to classify the intensity of infection as light, moderate or high, respectively (A. lumbricoides 1–4999, 5000–49 999 and > 50 000 EPG; for T. trichiuria 1–999, 1000–9999 and > 10 000 EPG; Hookworm, 1–1 999, 2 000–3 999 and > 4 000 EPG).

Determination of anaemia and nutrition status

Haemoglobin concentrations (Hb), height and weight were also measured. Haemoglobin levels were measured on-site using HemoCue Hb 301 (Hemocue AB, An-gelholm, Sweden), height and weight measurements were also taken on site following WHO standard protocol (de Onis et al. 2004). The children were measured in light clothing without shoes, hats or accessories. Weight was measured with a calibrated electronic scale. Height was measured using a standard tape, ensuring that the weighing station was set up on level ground to ensure accuracy of the equipment.

Assessment of school performance and cognitive ability

End of term test scores in Mathematics and English for the two previous terms were collected and compared. In addition, the participants were subjected to two core sub-tests on working memory and processing speed. Since research suggests that children’s working memory and processing speed are those areas of cognitive ability most likely to be affected by STH infection (Shang 2011), each participant was individually administered two core sub-tests. The two core sub-tests were letter-number series and digit span test. For letter number series, the raw scores were recorded as time taken in seconds, while the raw scores for digit span were recorded out of 32. These scores were then compared in STH infected and the uninfected children.

Data analysis

The collected data was first entered and cleaned in Microsoft excel and then analysed using SSPS version 22. Proportions were determined at 95% confidence interval and Chi-square test was used to ascertain association of low cognitive abilities, academic performance, sex and age with STHs. For variables whose expected frequencies was less than 5, Fishers exact test was used. Logistic regression was used for multivariate analysis. A significant level of 5% was used for all analyses.

Ethical considerations

The research was approved by the University of Zambia Health Sciences Research Ethics Committee (UNZAHSREC) (Ref ID: 202,112,030,104). In addition, permission was also obtained from the Lusaka district education office, school administrators, district medical office and the local health facility. Written informed consent and assent were also sought from each participant and their parents/guardians, respectively after explaining the study objectives and data collection methods. Confidentiality and anonymity were ensured, and participants found positive were followed up and treated.

Results

Characteristics of study participants and prevalence of STHs

A total of 209 samples were collected from school children with an age range of eight to 16 years, majority of the children were 13 years old. When categorised into two age groups, most of the children (55.5%; 116/209) were in the younger age group (8–12 years), the rest were in the 13–16 years age bracket. Out of the 209, majority were females (65.6%; 137/209). The children were from different classes (grades 2–9), however, most of them were from the 7th grade (Table 1).

Table 1.

Prevalence of STHs in school aged children (n = 209)

Variable	No sampled	Number + (%)	P value
Sex
Male	72	7 (9.7)	0.021
Female	137	3 (2.2)
Age group (yrs.)
8–12	9 (7.8)	9 (7.8)	0.022
13–16	1 (1.1)	1 (1.1)
Grade
2	18	1 (5.6)	0.082
3	26	3 (11.5)
4	24	3 (12.5)
5	17	2 (11.8)
6	24	1 (4.2)
7	59	0
8	8	0
9	33	0

The overall prevalence of STHs among the children was 4.8% (10/209; 95% CI: 2.3–8.6). The prevalence was significantly higher in males (9.7%; 7/72) compared to females (2.2%; 3/137) (p = 0.021). The younger children aged 8–12 years had a higher prevalence of STHs compared to the older children (Table 1) (p = 0.022). The parasites detected included A. lumbricoides (5), hookworm (4), and Strongyloides stercolaris larvae (1). Taenia spp and Schistosoma mansoni were also detected in one and two other children, respectively. From the schools included in the study, 90% of the STHs positive children were from the community school.

Association of STHs, anaemia and nutritional status

Haemoglobin concentrations (Hb) were measured for all the children included in the study to determine anaemia status and relate it to STHs infections. The height and weight were also measured and used to determine the Body Mass Index. Over 90% of the children had normal Hb levels according to their age specifications, only two children (females aged 8 and 12 years) had Hb level below the normal range (10 to 15.5 g/dl) but were negative for STHs. Regarding BMI, 91 (43.5%) children were under-weight while 5 were obese, however, most of the children were within normal ranges based on WHO identified normal figures for age and sex. Soil Transmitted Helminths were detected in seven of the healthy children (7/94) while three were from underweight children (3/91), the difference was however, not statistically significant (p = 0.375). Ascaris lumbricoides and hookworm were detected in both the underweight children (3 and 2 respectively) and those with normal BMI (hookworm 3; A. lumbricoides 2).

Association between STHs and cognitive function

End of term test scores in Mathematics and English for the two previous terms were collected and compared. The scores ranged from 8%-100% for both Mathematics and English. Interestingly, none of the STHs positive children obtained a score of 100% in both subjects, the school average score was 50% (range 18–78%) for Mathematics while that for English was 42.1% (range 16–70%). When the scores were categorised in five groups (with 20 points interval) and infection status compared in the groups, there was no significant difference in the scores between the infected and the non-infected children (p = 0.416). The results were similar with the English scores (p = 0.568).

The participants were further subjected to two core sub-tests on working memory and processing speed. Working memory is the ability to maintain activated knowledge in the focus of attention (Engle et al. 1999). Processing speed is a measure of the time taken to respond to and/or process information in one’s environment (Horning and Davis 2012). These scores were categorised into four groups (1–5; 6–10, 11–15, 16–20) and compared in STH infected and the uninfected children. There was no significant difference in working memory between the infected and uninfected (p = 0.604). On the other hand, the processing speed was categorised into six levels (Table 2), similarly, there was no statistically significant difference between the infected and the uninfected children. Results were similar with the scores attained by the children (Table 2).

Table 2.

Association between STH infection and working memory, processing speed and test scores among school aged children (n = 209)

Variable	No sampled	Number + (%)	P value
Memory
1–5	48	4 (8.3)	0.604
6–10	68	3 (4.4)
11–15	64	2 (3.1)
16–20	29	1 (3.4)
Processing speed (Secs)
0–50	69	2 (2.9)	0.497
51–100	104	5 (4.8)
101–150	21	2 (9.5)
151–200	4	1 (25)
201–250	5	1 (20)
250–300	1	1 (100)
Mathematics scores
0–20	11	1 (9.1)	0.416
21–40	56	5 (8.9)
41–60	93	3 (3.2)
61–80	43	1 (2.3)
81–100	6	0
English scores
0–20	16	1 (6.3)	0.476
21–40	42	4 (9.5)
41–60	84	4 (4.8)
61–80	48	1 (2.1)
81–100	18	0

Discussion

The current study investigated the prevalence of STHs in school aged children and whether this affected nutritional status and impaired cognitive function in Zambia children. The prevalence of soil-transmitted helminthiasis differs from region to region and within country variations are also very common. The overall prevalence of STHs was 4.8%, relatively lower compared with previous proportions that have been reported in various parts of Zambia (Siwila et al. 2010; Halwindi et al. 2017; Tembo et al. 2019). However, the previous studies by Siwila et al. (2010) and Halwindi et al. (2017) were in pre-school children with a different sample size and in different geographical locations, which could explain the differences. Majority (90%) of the STHs positive children were from a community school. Further interrogation indicated that the school did not participate in the school-based deworming programmes that public schools had previously participated in, three months prior to sample collection. According to the World Health Organisation, school age children (aged 5–14 years) are among the high-risk groups for STH infections, the others being pre-school children and women of reproductive age (WHO 2011, 2017). The prevalence tends to decrease with increasing age making school age children the most vulnerable. In this study, the prevalence of STHs was significantly higher in children aged 8–12 years, corroborating with the WHO report and a review report from India which indicated a high prevalence (62.5%) in children aged 6–12 years (Salam and Azam 2017).

Soil transmitted helminth infections have previously been reported to be higher in males than in females (Dahal et al. 2019; Mahapatra et al. 2020; Eltantawy et al. 2021). We found similar results with the boys having a prevalence of 9.7% compared to 2.2% for females. Investigative behaviour of boys with a view to explore the environment has been attributed to the high prevalence of STHs compared to female children that are more likely to be engaged in household chores (Odinaka et al. 2015; Dahal et al. 2019). Ascaris lumbricoides was commonly isolated followed by hookworm. Trichuris trichiura was not detected in this study. Many other studies have reported Ascaris lumbricoides to be widespread (Tabi et al. 2018; Dahal et al. 2019; Bah et al. 2019), however, a recent Tanzanian study reported a lower prevalence of A. lumbricoides compared to other helminths detected (Eltantawy et al. 2021).

The study further intended to determine if there was any association between STH infection and low Hb levels. Majority of the children (> 90%) had normal Hb levels according to WHO identified normal range for age (8–16 years in this study) and sex (WHO 2007). The only two children with low Hb levels were negative for STH infections. Anaemia can be caused by a number of factors which were not investigated in this study. The nutritional status was determined based on the BMI, 43.5% children were under-weight, three of these had STHs, however, the infection status in the various categories were not statistically significant from those in underweight children. Many variables can affect BMI in children, and these have extensively been explored by various researchers (Braithwaite et al. 2014, 2017; Murphy et al. 2014, 2015; Hancox et al. 2015; Mitchell et al. 2017, 2018; Wall et al. 2018). Further, it has long been recognised that intestinal parasite infections and undernutrition are closely linked (Stephenson et al. 1994; Papier et al. 2014; Cossa-Moiane et al. 2022). This was, however, not evident in the present study, conclusions cannot therefore be made due to the small number of cases in the school children and the sample size. In addition, the observed Mathematics and English scores had no relationship with STH infection in the school children. In comparison, a study in China observed that STH infection was associated with worse cognitive ability, nutritional status and school performance (Liu et al. 2015).

School age children (aged 5–14 years) are among the high-risk groups for STH infections (WHO 2011, 2017). Prevention and control of infection in this group would therefore eliminate the health effects associated with of such infections. The successful control of STHs in areas where they are no longer a problem (the United States of America, South Korea, and Japan) was largely dependent on WASH improvements and structured deworming (Vaz Nery et al. 2019); adopting these in low to middle-income countries such as Zambia would help reduce infections in high-risk groups. However, low to middle income countries have overcrowded communities with insufficient sanitary facilities and limited access to water, which makes it difficult to effectively implement WASH.

Conclusions

Soil Transmitted Helminths are prevalent among school children in the study area with A. lumbricoides being the most common. The parasites are more common in boys than in girls. It is evident that deworming can significantly reduce infections as was observed in public schools where prevalence was significantly low. There is need for further large-scale studies to understand the relationship between STHs and cognitive function in school age children in Zambia.

Author contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by Daughter Jumbe. Data analysis was done by Daughter Jumbe and Joyce Siwila. The first draft of the manuscript was written by Daughter Jumbe and both authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Data availability

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

Declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of the University of Zambia School of Health Sciences (Ref ID: 202112030104).