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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 27  |  Issue : 3  |  Page : 184-189

Soil-transmitted helminthiasis: A neglected tropical disease among urban slum dwelling school-aged children of a sub-Saharan African city


1 Department of Paediatrics, University of Nigeria Teaching Hospital; Department of Paediatrics, Niger Foundation Hospital, Enugu, Nigeria
2 Department of Paediatrics, University of Nigeria Teaching Hospital; Department of Paediatrics, College of Medicine, University of Nigeria, Enugu, Nigeria
3 Department of Internal Medicine, Mental Health Unit, NnamdiAzikiwe University, Nnewi, Anambra State, Nigeria

Date of Submission19-Feb-2020
Date of Decision19-Apr-2020
Date of Acceptance21-Apr-2020
Date of Web Publication17-Jul-2020

Correspondence Address:
Dr. Adaeze Chikaodinaka Ayuk
Department of Paediatrics, College of Medicine, University of Nigeria, Enugu Campus, Enugu
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/npmj.npmj_38_20

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  Abstract 


Background: The need to generate a robust epidemiological data on the neglected tropical diseases is imperative, in order to encourage access to formal care, drive public policies and ensure the allocation of resources by policy-makers. Objectives: The objective of this study was to determine the prevalence of soil-transmitted helminthiasis (STH) and its association with nutritional variables among primary school pupils living in urban slums in a South-Eastern sub-Saharan African city of Enugu, Nigeria. Methods: The stool samples of school-aged children living in urban slums were analyzed for ova of the helminths using the Kato-Katz methods, whereas the nutritional assessment (weight and height) was obtained and analyzed to indicate acute or chronic malnutrition. Degrees of helminthic load were then classified. The socioeconomic status was determined while the prevalence of STH and the relationship between it and the nutritional stratus was assessed to ascertain any significance between being malnourished and having STH as this will inform policy decisions. Results: There were a total of 371 analyzed stool samples from 228 females (61.5%) and 143 males (38.5%), with 285 (76.8%) from the lowest socioeconomic class. The prevalence of STH was 18.1%, while that of acute and chronic malnutrition were 3.3% and 7.5%, respectively. The intensity of infestation was, however, light, with the highest mean egg intensity of 74.4 ± 32.8 documented for ascariasis. There was no statistically significant association between the presence of STH and various indices of acute and chronic malnutrition (P > 0.05). Conclusion: STHs prevalence is high among children living in urban slums. Nutritional status was, however, not adversely affected by helminthic infestation.

Keywords: Children, neglected, slums, soil-transmitted helminthiasis, tropical


How to cite this article:
Ohuche IO, Ayuk AC, Ubesie AC, Onu JU, Ibe BC. Soil-transmitted helminthiasis: A neglected tropical disease among urban slum dwelling school-aged children of a sub-Saharan African city. Niger Postgrad Med J 2020;27:184-9

How to cite this URL:
Ohuche IO, Ayuk AC, Ubesie AC, Onu JU, Ibe BC. Soil-transmitted helminthiasis: A neglected tropical disease among urban slum dwelling school-aged children of a sub-Saharan African city. Niger Postgrad Med J [serial online] 2020 [cited 2020 Aug 11];27:184-9. Available from: http://www.npmj.org/text.asp?2020/27/3/184/289912




  Introduction Top


Globally, over 1.5 billion people are infested with soil-transmitted helminthiasis (STHs), with sub-Saharan Africa, accounting for about 41 million hookworm-infested children of school age. About 85.5 million African school-aged children required preventive chemotherapy for STH in 2014.[1],[2],[3] The common STH species of major public health challenge among children in developing countries include Ascaris lumbricoides, hookworms (Ancylostoma duodenale and Necator americanus) and Trichuris trichiuria.[4],[5]

Malnutrition remains an important public health issue with stunting prevalence of 37.0%, and an 18.0% overall prevalence of wasting in Nigeria.[6],[7] Inadequate intake of food as a result of poverty and insufficient household food security which are risk factors for malnutrition have been known to be associated with a higher prevalence of STH.[4],[8],[9] Strategies to improve nutritional status must thus focus on possible relevant aetiologies of malnutrition, including STH.[8],[9],[10]

There is a paucity of information regarding the impact of these STH on the nutritional status of children in the most vulnerable areas. This study sought to highlight the current prevalence of STH among primary school children in the most vulnerable areas of our locality and to assess the relationship between infestation with STHs and nutritional status.


  Methods Top


Ethical consideration

Ethical approval was sought and obtained from the Health Research Ethics Committee of University of Nigeria Teaching Hospital, Ituku-Ozalla on 22nd June in 2016, before the commencement of the study. Signed or thumb printed informed consent was obtained from the parents/caregivers, whereas assent was obtained from children aged 7 years and above.

Study design

This was a school-based, descriptive cross-sectional study of eligible school-aged (6–12 years) children attending primary schools in urban slums in Enugu, South-east Nigeria.

Study area

We studied children living in urban slums in Enugu. Enugu urban area consisting of Enugu North, Enugu South and Enugu East local government areas has a total of 14 slums,[11] – Obiagu, Ugwu Aaron, Ugwu Alfred, Udi Siding, OlogoNgwo, Ikirike, Garriki, UgboEzeji, Ugbo Nchanawu, Ugbo Paul, Ugbo Okonkwo, Agu Abor Hill, UgwuAgor and Mkporogwu. These slums are high-density areas with a lack of potable water and lack of proper sewage disposal measures. They, therefore, fit into the United Nation's-Habitat operational definition of urban slums as follows: 'Urban slums are areas that possess inadequate access to safe water, inadequate access to sanitation and other urban infrastructure, poor structural quality of housing, overcrowding, and insecure residential status, or a subset of these characteristics'.[12]

Sampling size and collection, procedure

The minimum sample size was determined based on a standard statistical formula[13] for prevalence rates n = Z2.p.(1 − p)/d2, where n = minimum sample size, p = observed proportion 0.326 (From the study by Ilechukwu et al. on the relationship between nutritional status and infection with common intestinal helminths in primary school children).[14]Z = value of the standard normal distribution 1.96. d = desired precision 0.05. Therefore, n = (1.96) 2 (0.326) (0.674)/(0.05) 2 = 337.

Non-response rate was approximated to 10%, giving a total sample size of approximately 370.

Data collection occurred over an 8-month period (August 2017–March 2018). A multistage sampling technique was used in selecting the study participants. In the first stage, the 14 slums in Enugu urban were stratified into local government areas. Enugu North had a total of 2 slums; Enugu East had 7 slums, while Enugu West had 5 slums. One slum was selected from each local government area using the simple random sampling by balloting, giving a total of three selected slums. In the second stage, a school was chosen from each selected slum. Since the three slums selected had only one public school each, this public school was selected for the study. The calculated sample size of 370 was allocated proportionately to each school, depending on the size of the school, as shown in [Table 1]. Obiagu Primary school from Enugu North Local Government area has a total population of 210 pupils and was allotted 102 samples. Hill side primary school from Enugu East had a total population of 110 pupils and was assigned 52 samples, whereas Idaw River Primary School from Enugu West had a total population of 440 pupils and was allotted 214 samples. The sample size for each school was then allocated proportionately to each class in the school, based on the total number of children in each class. To select the particular children to be enrolled in each class, a systematic random sampling technique using the class register was employed. For each class, the sampling frame (interval) was calculated using the total number of pupils in the class divided by the number needed from the class. The first person was selected by using simple random sampling by balloting and the subsequent by the nth number according to the sampling interval for the class. This was repeated for all the classes until the required sample size was obtained. Selected children were given consent forms for their parents, and the study and its requirements were also explained in the English and the local language to the students by the researcher, with the help of the class teachers. Parents who signed consent forms were followed up for the completion of the interviewer-administered questionnaire, either at home or in their work place. In addition, some parents, especially parents of the younger children, were interviewed during school runs in the morning or in the afternoon, as they came to drop-off, or pick their children from school. Before the completion of the questionnaire, parents were questioned for the exclusion criteria. Parents of children who had any chronic illnesses, had lived in the study area for <6 months or were dewormed within the 3 months before the study were not interviewed, and the children were not enrolled in the study. Parents of children who met the inclusion criteria were interviewed, and their children enrolled. Assent was obtained from the children whose parents filled the consent forms. All parents who gave consent for the study participated in the study after it was explained in detail to them and their questions and doubts addressed. Subsequently, the second section of the questionnaire which was also interviewer-administered was completed by the child, and their weights and heights were then measured. Finally, they were given a clean specimen bottle for stool collection.
Table 1: Disposition of population of study participants following a multistage sample

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Stool collection and analysis

Following informed written consent, a clean, properly-labelled, wide-mouthed, dry and leak-proof unbranded specimen container was given to each participating child for stool specimen collection. Each specimen bottle was properly labelled with the participant's identification number. Pupils were instructed to collect fresh, early morning stool samples in the specimen containers, to be submitted on arrival at school. A single stool sample from each participant was used for the analysis of ova of intestinal helminths. Stool samples were collected from the pupils on weekdays, and then transported to the laboratory within 1 h of collection. Stool samples were preserved at room temperature in the laboratory, and slides were prepared and read within 6 h on the same day. Stool analysis was carried out by means of the Kato Katz method. Using this method, faecal specimens were pressed through a mesh screen to remove large particles, then a portion of sieved sample was transferred to the hole of a template on a slide.[15] After filling the hole, the template was removed, and the remaining sample covered with cellophane soaked in glycerol, which clears faecal matter from around the eggs.[15] The slides were viewed under a microscope with a magnification of ×10, and ×40 with the help of a parasitologist. The eggs were then counted, and the number of eggs per gram (epg) of faeces calculated.

Data management and analysis

The data obtained were entered into the Statistical Package for the Social Sciences version 20.0 IBM Corp. Released 2011. IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY: IBM Corp. for analysis. First, data were scrutinized for incorrectly filled information and normality of distribution of data, using frequency counts and graphical displays. Thereafter, the results were displayed in frequencies, charts and tables as appropriate. Quantitative variables such as age and anthropometric indices were summarized using means and standard deviations (SDs), whereas qualitative variables such as gender, socioeconomic class (SEC) and nutritional status were summarized using frequency and percentages. Association between categorical variables was done using the Chi-square. Means of continuous variables were done using the independent test and ANOVA. The level of statistical significance was achieved if P < 0.05. Results were presented in tables and charts. Information regarding the parents' educational status and occupation, as well as the child's biodata and clinical history was obtained using a semi-structured questionnaire. Socioeconomic status of parents was determined using Oyedeji's classification.[16] This was based on the mean of a set of scores, assigned for the educational attainments and occupation of parents. A score of 1–5 was assigned to each education or occupation category. The mean of the four scores was approximated to the nearest whole number, and this was the social class assigned to the child. The assigned SEC was then further classified into upper (I and II), middle (III) and lower (IV and V) socioeconomic groups.[16] Anthropometric measurements, including weight and height, were obtained using standard methods.[17 -19] All anthropometric measurements were carried out in duplicates. The mean of the two readings was then calculated and used for analysis.[20] Age, weight and height were used to calculate the height-for-age Z-score (HAZ) to assess stunting; and body mass index (BMI)-for-age Z-score (BAZ) to assess thinness. Calculations were done with the World Health Organisation (WHO) Anthro software,[21] using the WHO international reference values. Values obtained were compared to the recommended 2007 WHO growth chart standard. BAZ was used as a complement to HAZ because weight-for-age Z-score is not recommended for the assessment of growth beyond 10 years of age, since it does not distinguish between height and body mass in this age group.[19] According to the WHO growth reference for school-aged children and adolescents, underweight is defined as weight for age <–2 SD of the WHO child growth standards median, stunting is defined as the height for age <–2 SD of the WHO child growth standards median, wasting is defined as the weight for height <–2 SD of the WHO Child growth standards median overweight is defined as the weight for height >+2 SD of the WHO child growth standards median, whereas thinness and severe thinness are defined as a BMI Z-score score <−2 and −3 SD of BAZ, respectively.[17],[21],[22] In accordance with the WHO classification,[23],[24] data on the intensity of infection were classified into light (<4999 epg for ascariasis, <999 for trichiuriasis and <99 for hookworm), moderate (<49,999 epg for ascariasis, <9999 for trichiuriasis and <3999 for hookworm), and heavy (≥50,000 epg for ascariasis, ≥10,000 for trichiuriasis and ≥4000 for hookworm), and this was represented mean epg of stool in tabular form, [Table 2].
Table 2: Description of the helminthic load among the study participants

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  Results Top


A total of 371 children aged 6–12 years were enrolled in the study, of which 228 were female (61.5%) and 143 were male (38.5%), as shown in [Table 3]. Majority (285; 76.8%) of these urban slum dwelling children belonged to the lowest SEC. Ova of helminths were identified in 67 out of 371 stool samples analysed (18.1%), with a predominance of ascariasis. The prevalence of the other soil transmitted helminths is shown in [Table 4]. The intensity of infestation was noted to be light, as shown in [Table 2].
Table 3: Sociodemographic characteristics of study participants

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Table 4: Prevalence of soil-transmitted helminthiasis among the study participants

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The analyses of anthropometric indices showed that 355 (95.7%) children had a normal BAZ, whereas 343 (92.5%) children had a normal HAZ. Twelve (3.3%) children were undernourished, whereas 4 (1.1%) were overnourished [Table 5]. Out of the 67 children with helminthiasis, 62 (92.5%) had a normal nutritional status, while of 304 children without helminthiasis 293 (96.4%) had a normal nutritional status. Conversely, 8 out of the 12 children (66.7%) with undernutrition did not have helminthiasis. There was no statistically significant relationship between helminthiasis and nutritional status of the participants (χ2= 2.1 P = 0.34) [Table 6].
Table 5: Nutritional status of the study participants

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Table 6: Relationship between helminthiasis and nutritional status

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  Discussion Top


This study noted a high prevalence of STH infestation among children living in urban slums with a predominance of monoparasitism. Similar prevalence rates were also documented by some studies carried out in other parts of the country.[5],[14],[25],[26],[27],[28] Our study documented normal nutritional status in majority of the children with no significant association between STH infestation and the nutritional status as most had normal BMI Z-score irrespective of the STH status. This trend was documented by several other researchers[10],[26],[29] who carried out similar community-based nutritional surveys. Although infection with helminthiasis has been posited as a risk factor for malnutrition,[30] this current study did not find a positive association. The 7.5% prevalence of chronic malnutrition obtained in the present study was, however, higher compared to other surveys by Ilechukwu et al.[14] in Enugu with stunting prevalence of 0.2% and Igbokwe et al.[26] with stunting prevalence of 0.8%. Their study population were, however, not among children residing in slums. Conversely, Amuta et al.[27] in an urban-slum residential comparison in Makurdi, Nigeria, noted a higher prevalence of undernutrition among school children living in slums, thus explaining the comparative higher prevalence in our study. In the present study, all the helminths identified were of light intensity, as classified by the WHO. Ilechukwu et al.[14] equally documented a predominance of light helminthic infections in their study population. Ascariasis had the highest intensity in our study, whereas trichuriasis had the least intensity of infestation. The dominance of ascariasis has been documented in similar studies.[2],[31],[32],[33] This may be attributable to the large number of eggs (up to 200,000) shed daily by the adult worm, with additional features that render them resistant to adverse environmental conditions.[34]

Malnutrition is known to have many risk factors such as inadequate intake of food as a result of poverty and insufficient household food security; intake of poorly-balanced diets as a result of ignorance, as well the presence of coexistent childhood infectious diseases (such as STH).[4],[8],[9] These factors may be present in the child living within the urban slums. STH as a risk factor is however further dependent on the duration and intensity of infection, as well as the overall prevalence or burden of helminthic infection. The intensity of infection in all the children studied was light. This may be attributed to the fact that in the schools studied, it was noted that regular deworming of children by parents was a relatively common practice, which may have led to an overall reduction of the burden and duration of helminthic infections among these children. This may further explain the non-significant relationship between STH and malnutrition found in the current study. In line with this, Stephenson et al.[35] proposed that a significant association between helminthiasis and nutritional status may not be likely where the prevalence of helminthiasis is <20.0%, as is the case in the current study with a prevalence of 18.1%. Other researchers have also documented no significant association between helminthiasis and nutritional status. Ilechukwu et al.[14] who had an STH prevalence rate of 32.6% among nursery and primary school children in Enugu documented no significant difference in the weight-for-height and HAZ of children with helminthiasis, as compared to uninfected children. Similar to our study, majority of the children with helminthiasis in their study had light helminthic infection, which may have a negligible impact on nutrition, as opposed to moderate or heavy worm burdens. Degarege and Erko.[29] in Northwest Ethiopia also reported no significant difference in the prevalence of stunting between children with and without helminthiasis. Ahmed et al.[36] in Malaysia, Sarkar et al.[37] in Bangladesh and Sanchez et al.[38] in Honduras, however, found a significantly higher prevalence of malnutrition, among children with helminthiasis. Nevertheless, all three studies had very high prevalence rates of STH (>50%) among their study population, which is not the case with the index study. Moreover, some studies[38],[39],[40] have linked the association between malnutrition and helminthiasis with the prevalence of polyparasitism. The very low prevalence of polyparasitism in the index study (0.6%) may also explain the disparity between the findings of the current study and those of the afore-mentioned studies.


  Conclusion Top


This study documented a high prevalence of helminthiasis, which still remains a neglected tropical disease, among school-aged children living in urban slums. This requires proper health policies and intervention among these under-privileged children. Nutritional status was not adversely affected by helminthic infection, and therefore, malnutrition in the study population may be attributable to other aetiologies.

Acknowledgements

We thank all the participants of this study (both children and parents); we also thank Mr. C. Emeribe for his assistance with the laboratory work. Finally, we thank our research assistants Monica Udoh, NkechiEmelife, and UcheAgu, their inestimable help.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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