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Prevalence of intestinal parasites and associated risk factors in school-going children from informal settlements in Nakuru town, Kenya

Naomi M. Chege1*, Bartholomew N. Ondigo1,2,3, Frank G. Onyambu4,5, Alex Maiyo Kattam6, Nancy Lagat6, Tabitha Irungu7, Elizabeth Jemaiyo Matey7
1. Department of Biochemistry and Molecular Biology, Egerton University, Nakuru, Kenya
2. Laboratory of Malaria Immunology and Vaccinology, National Institute of Allergy and Infectious Disease, NIH, Bethesda, Maryland, USA
3. Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
4. Centre for Excellence in HIV Medicine Project, University of Nairobi, Kenya
5. School of Health Sciences, Meru University of Science and Technology, Meru, Kenya
6. Centre for Virus Research, Kenya Medical Research Institute, Nairobi, Kenya.
7. Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya


Abstract

Background

Intestinal parasites are a major public health problem in the developing world and have attracted increasing interest among health researchers within the past decade. Epidemiology-based studies have shown that their prevalence is high and frequently recur in regions with poor sanitation and inadequate sewerage facilities. We determined the prevalence of intestinal parasites, their intensities, and associated risk factors in an informal settlement.

 Methods

This was a cross-sectional study conducted in three randomly selected public primary schools located in Nakuru town informal settlements. A total of 248 stool samples from asymptomatic pupils were screened for infections with soil-transmitted helminths (STH) using the Kato Katz technique. A random subset of the stool samples (n=96) was also screened for intestinal protozoa using polymerase chain reaction (PCR). Socio-demographic variables were collected using a pre-tested structured questionnaire for the analysis of risk factors for infection.

Results

The overall prevalence of intestinal parasites was 17.3% (n=43). The overall prevalence of both STH and intestinal protozoa parasites was 1.2% and 41.7% respectively. The most diagnosed STH infection was Trichuris trichiura (1.2%) followed by hookworms 0.4% and Ascaris lumbricoides (0.4%). Intestinal protozoa parasites Entamoeba histolytica, Entamoeba hartmani, Entamoeba dispar, Giardia intestinalis and Entamoeba coli had a prevalence ranging from 0-38.5%. All the infections were light, with egg intensities <100 for each of the STH. Multiple infections prevalence for intestinal protozoa parasites was 5.2% (n=5) and 0.4% (n=1) for STH in the subset samples. Risk factors for intestinal parasitic infections included rearing of goat (p=0.046), earthen floor type (p=0.022), number of household rooms (p=0.035), and source of food (p=0.016).

Conclusion

The low prevalence of intestinal parasites in informal settlements of Nakuru may be attributed to improvements in hygiene and sanitation, deworming, and good health practices facilitated by the department of public health in the county.


 Introduction

Intestinal parasitic infections are a serious public health issue in developing countries despite being the most preventable and treatable diseases1. It is estimated that over 3.5 billion people globally host at least one intestinal parasite species leading to over 450 million disorders1. This bestows a considerable burden on health systems especially in the developing world where the majority of these infections occur. Intestinal parasites continue to affect human productivity by causing various medical complications. The complications range from abdominal pains, anemia, diarrhea, delayed growth, undernutrition, reduced physical activity to impaired cognitive development in young children2,3. Epidemiological-based surveys have shown that these parasites recur in regions with poor sanitation and hygiene facilities such as in informal settlements in developing countries4.

The rural-urban migration in the context of economic strains and search for better jobs has engineered the growth of informal settlements and over time, they have become the home of a substantial number of city residents5. The affordable housing attracts low-income earners in the cities and result in overcrowded unhygienic environments and strained basic necessities and consequently limited government services access3,6. The poor drainage systems, heaps of garbage, indiscriminate excreta disposal such as wrap and throw, and shared pit latrines continue to pose a greater health risk to the inhabitants as population increases6. Contamination of water sources, food, and environment with pathogens that flourish in such unkempt environments remain inevitable and infect humans through the fecal-oral route7,8. Pre-school and school-aged children inhabiting informal settlements are at a higher risk of acquiring these infections since they rarely observe hygiene, are active and play in contaminated environments and households, and often practice indiscriminate eating habits9,10.

The spread of intestinal parasitic infections is further enhanced by the presence of healthy carriers who form a parasite reservoir for future infections leading to continuous and persistent disease endemicity10. Recent molecular epidemiological studies have addressed potentially pathogenic intestinal protozoa parasites considered non-pathogenic for many years. Entamoeba dispar, E. hartmani and E. moshkovskii have been recovered from patients with gastrointestinal symptoms11,12 and E. coli in clinical symptoms where no other parasitological or bacteriological agents were found13. This suggests that commensal Entamoeba spp. could be pathogenic and of clinical importance. There is, therefore, a need to re-evaluate the epidemiology of intestinal protozoa parasites in terms of morbidity particularly in those geographical areas thought to be highly endemic. The study determined the prevalence, intensity, and risk factors associated with intestinal parasites among asymptomatic school-going children in informal settlements of Nakuru town.

Materials and Methods

Study design, setting and study subjects

This cross-sectional study was conducted in informal settlements of Nakuru town, the fourth-largest urban center in Kenya, covering an estimated area of 7,496.5km2 14. Nakuru consists of fifteen wards within its locality and is categorized into low-income areas (informal settlements) with high population densities, middle-income areas with medium population densities, and high-income areas with low population densities. Over 50% of people living in Nakuru town live in informal settlements (including London, Gioto, and Kaptembwa)14. The town continues to witness a tremendous increase in population due to its cosmopolitan nature, fertile agricultural hinterland, central strategic location, and job opportunities vicinity15. Due to lack of space, the town boundary lies between the scenic Menengai crater to the north and the Lake Nakuru to the south. Most migrants settle in the already over-crowded unplanned informal settlements, which continues to experience a strain in basic amenities.

The study participants were asymptomatic children aged 8-13years from 3 randomly selected primary schools (Kaptembwa, Milimani, and Prisons) located in informal settlements of Nakuru town. The choice of study participants was based on their age group which is considered at high-risk of infection and are capable of responding to the questionnaire administered to understand the correlates of infection. The study participants were sampled randomly and about 20% additional children (from the sample size) were included to cater for the pupils who may not have returned samples or those absent from schools during sample collection. We excluded children whose parents did not consent for inclusion in the study and those who could not provide stools at the time of sample collection.

 Sample and data collection

Sample collection from children in the three schools was done in June 2018. The purpose of the study was explained to the children and teachers before the issuance of consent forms two weeks prior to sample collection. Teachers assisted the children to acquire consent from their parents. On the morning of sample collection, sterile Ziploc aluminum bags labeled with unique identity were issued to each study participant who had consented. An oral description on use and proper handling of the stool bag and specimen was given. Each child provided a single stool sample for diagnosis. The fresh stool samples were transported to Langa Langa sub-county hospital laboratories in cooler boxes immediately following collection for processing. A pre-tested structured questionnaire was then administered to gather demographic data and other variables from the participants. Core questions on water, sanitation, and hygiene in households were captured in the questionnaire. The officer-in charge of public health confirmed that they had not dewormed the children in schools three months prior to the study period (Gachahi CW, 2018, personal communication).

Laboratory screening by Kato Katz and polymerase chain reaction

Soil-transmitted helminths were detected using the Kato Katz technique and intestinal protozoa parasites using polymerase chain reaction (PCR). Kato Katz technique involved the preparation of two thick smears from each stool sample and microscopic examination for T. trichiura, A. lumbricoides, and hookworm for the presence of egg(s) and intensity of infection16. The intensity of infection was determined based on parasite-specific egg counts and the count adjusted to eggs per gram (epg) of feces. Each slide was observed within 60 minutes of preparation by two independent, experienced microscopists. A laboratory supervisor randomly crosschecked 10% of the slides for quality control purposes. The intensity of infection was categorized as light, moderate or heavy according to the World Health Organization (WHO) proposed thresholds17.

Molecular detection of intestinal protozoa parasites was done using approximately 0.2g of feces from a subset of randomly selected samples (n=96) preserved in 0.8ml DNAzol® (Molecular Research Center, Inc., OH, USA). Molecular analysis was done at Kenya Medical Research Institute (KEMRI) Nairobi, Center for Microbiology Research (CMR) molecular laboratory. Extraction of DNA was done using DNAzol® according to the manufacturer’s instruction and used for screening of Entamoeba sp. (E. histolytica, E. hartmani, E. dispar and E. coli) and Giardia intestinalis. Entamoeba sp. presence was detected with an initial universal nested polymerase chain reaction (PCR), followed by subsequent species-specific PCRs targeting the 18S ribosomal RNA subunit gene as previously explained by18. Giardia intestinalis was detected via a nested PCR targeting the glutamate dehydrogenase gene (GDH) as previously described by19. All PCR products were resolved on an ethidium bromide-stained 1.5% agarose gel in Tris-Acetate-Ethylenediaminetetraacetic acid (TAE) buffer and the amplicons visualized under ultraviolet light. Intestinal protozoa parasites detection and prevalence was based on band size. All data were tested for normality prior to statistical analysis.

Data management and analysis

Data were entered into Microsoft Excel sheet and crosschecked with questionnaires to ensure accuracy. All statistical analyses were performed using SPSS software system, version 20 (IBM Corp., Armonk, N.Y., USA). Frequencies and proportions were used to describe the demographic characteristics of the study population. A comparison between children infection status and risk factors for intestinal parasitic infections was performed using crosstabs. Pearson’s correlation and univariate analysis were used to determine the association of intestinal parasitic infections to the risk factors. Stepwise multiple linear regression was done on all risk factors analyzed against intestinal parasitic infections. The statistical significance level used was p <0.05.

Ethical consideration

The study was conducted in conformity to Declaration of Helsinki and International Conference in harmonization regulations. Approvals were sought from the Kenya Medical Research Institute (KEMRI) Science and Ethics Review Unit (SERU), Nakuru county health and education offices, and from respective school headteachers. Written consent was also sought from each participant guardian/parent with the consent form clearly indicating the study purpose, any anticipated consequences of the research, the anticipated uses of the data, possible benefits and harm, data confidentiality and the option to withdraw their children participation at any given time. Children found positive for any intestinal parasite received treatment as per the Ministry of Health (MoH), Government of Kenya guidelines.

Results

Study population characteristics

A total of 248 (female 56.9%) children aged 8-13years with a median age of 10years were enrolled in the study. Ten children did not provide stools at the time of sample collection. Two-thirds (66.5%) of the participants did not have a defined way of disposing garbage and was left scattered in the environment. Almost two-thirds (64.1%) of the residents used shared toilets.  About three-quarters of the residents (73.4%) had access to piped-tap water while others used water from wells (2.1%), water vendors (8.9%), and rainwater (14.1%). The majority of the participants (56.1%) treated drinking water, 34.3% boiled drinking water and 5.7% drank untreated water. Less than quarter of the participant’s parents/guardians were unemployed (15.7%) with the rest being either farmers (3.6%), formally employed (27.4%), informally employed (16.5%), or businesspersons (30.7%). Sixty-nine percent of the children had lunch prepared in their respective schools (table 1).

 

Prevalence and intensity of STH and intestinal protozoa

The overall intestinal parasites prevalence was 17.3%, (n=43). Soil-transmitted helminths were observed in 1.2%, (n=3) of the study population. The most detected STH was Trichuris trichiura, 1.2%, (n=3) followed by hookworm 0.4%, (n=1) and Ascaris lumbricoides 0.4%, (n=1) (table 2). The infection intensities were light with mean intensities of 10, 69, and 14 epg being observed for T. trichiura, A. lumbricoides, and hookworms respectively. The randomly selected subset of participants (n=96) screened for intestinal protozoa parasites, 41.7%, (n=40) tested positive for at least one of the three parasites (E. dispar, E. coli and G. intestinalis). The individual prevalence of E. histolytica, E. hartmani, G. intestinalis, E. dispar and E. coli was 0%, 0%, 4.2%, 6.3% and 38.5% respectively (table 2). Multiple infections for STH were observed in one of the 248 children in the study (0.4%). In addition, from the 96 randomly selected children, multiple intestinal protozoa parasites infections were recorded for 5.2% (n=5) individuals (table 3).

Risk factors associated with intestinal parasitic infections

Intestinal parasites were similar between females and males (16.3% and 15.9%: p=0.928).  Though not significant, infection rates were higher in age groups 8 – 9 years (20%) and 12 – 13 years (19.4%) as compared to 10 – 11 years (14.4%) (table 4). Prevalence of intestinal parasites decreased with an increase in the number of household rooms (Figure 1) (p=0.035) while children who had lunch prepared in school had a lower infection levels (12.4%) as compared to those who ate home-packed lunch (24.7%) (p=0.016). Further, a majority of children who lived in earthen floor (p=0.022) households and those who reared goats (p=0.046) had a higher chance of being diagnosed with STH. Subsequently, children who used rainwater for drinking were more likely to have intestinal protozoa parasite infections (p=0.052) than those who used tap water, bought water from vendors, or used water from wells. Stepwise linear multiple regression revealed a reduction in intestinal protozoa parasites infections with an increase in parent employment (p=0.012), less congested households (p=0.014) and eating food prepared in school (p=0.023) while food source (p=0.021) influenced both STH and intestinal protozoa parasites (intestinal parasites) (table 5). The number of rooms as a major risk factor to intestinal parasitic infections was significantly influenced by the type of household floor (p=0.002), number of people living in the household (p=0.004), and parent occupation (p=0.024) (table 5).

Discussion

Reliable estimates and updates on the status of intestinal parasites in vulnerable regions are important to guide control. Our findings on intestinal parasitic infections report a 17.3% overall prevalence among school-going children from informal settlements of Nakuru town. Higher prevalence of intestinal parasites has been reported from similar settings in Thika (>48.9%)20 and Nairobi (25.6%)21, Nigeria (86.2%)22, and Pakistan (52.8%)23. The differences in prevalence could be attributed to the detection methods used, the socio-economic activities, ecological and environmental differences2. In addition, improvements in sanitation, hygiene, and infrastructure supported by World Bank in regions of Kaptembwa and Milimani, that was ongoing, and public health education by the department of health at the county (Gachahi CW, 2018, personal communication) could have contributed to the low prevalence. These improvements facilitated proper and safe ways of garbage disposal and toiletry facilities in addition to enhanced water supply and hand washing facilities that synergistically decreased intestinal parasitic infections and transmission. The low prevalence of intestinal parasites suggests low environmental contamination with the infective pathogens. The very low multiple infections could be explained by the fact that these rarely remain asymptomatic and may not be diagnosed in the study’s asymptomatic population. However, low infection intensities of intestinal parasites, infection duration, and the immune status of the child may influence the appearance of symptoms in infected and co-infected children24.

The prevalence of STH infections reported in urban informal settlements of Kenya ranged between 34%-40.7% 3,25,26 which was incomparable to our study findings of 1.2%. This could be explained by the fact that most of these studies on STH in Kenya have been conducted in areas already reported to be endemic for the infections. Prevalence of STH are always influenced by climate (humidity, temperature, rain) and soil factors; hookworm transmission for instance, peaks at temperatures around 40°C27.

The overall Intestinal protozoa parasite infections were (41.7%), E. coli, E. dispar and G. intestinalis (38.5%, 4.2% and 6.3% respectively). Predominance of E. coli and E. dispar is common in tropical regions and their implications in chronic and subclinical human disease mechanisms have not been well studied28. Indeed E. dispar is often misdiagnosed microscopically29 and in immunodiagnostics for E. histolytica30. Entamoeba coli has also been associated with abdominal fat deposition in children suggesting possible long-term implications31. Prevalence of E. histolytica in this study is consistent with what is reported in other regions of Kenya(<1%)(32), Indonesia(0%)11, and Peru(0%)33 done on asymptomatic children. The prevalence of Giardia intestinalis reported here was consistent with an earlier study34 in informal settlements of Nairobi using similar diagnostic methods.

Food and food handler’s hygiene is an important factor in the transmission of intestinal parasites35. Taking lunch prepared in school minimized intestinal parasitic infections. Teachers and matrons in schools are the caregivers who ensure that children observe basic hygiene practices. The home-packed lunch is subject to contamination because the food containers may not be properly cleaned and sealed. Consequently they may pack leftovers and food prepared along the streets or unwashed fruits which may be unhygienic36. Food displayed along the streets attracts flies that transfer cysts, eggs, and larvae of intestinal parasites contaminating the food and posing a serious threat to children37. In addition, limited water sources and socio-economic status of the majority of informal settlements inhabitants’ increases the possibility of cross-contamination of water supplies. Rainwater for instance, has been shown to increase the likelihood of intestinal protozoa infections in this study. Its contamination may occur along the household roofs, collection pipes, in storage tanks, from animal droppings as they are reservoirs of intestinal protozoa parasites38 and in the process of transportation39 to the households from collection tanks. Besides, G. intestinalis, a majorly water-borne protozoa, can survive very low temperatures like of collection tanks and is often resistant to water treatment procedures like chlorination10.

Low socioeconomic factors are a known risk factor for intestinal parasitic infection40. Household overcrowding as observed in our findings increases intestinal parasites and has been previously reported in children between 0-16years41. Programs based on reducing household overcrowding have evidently minimized infections41. This is consistent with our present study as a significant reduction of intestinal parasitic infections was reported in less congested households (between 4-6 rooms) and in households where parents were employed. Overcrowding in houses increases the potential spread of intestinal parasites from an infected to a healthy person by increasing transmission per contact40. Smaller overcrowded households are associated with a strain in basic amenities such as water42 suggesting that such chores are rather underdone or foregone. Unemployed parents may experience a strain in their budget and therefore prioritize other basic necessities at the expense of observing hygiene. It is also possible that unemployed individuals were likely to be illiterate which has been associated with increased intestinal parasitic infections40. Earthen floor in overcrowded households also increased the risk of intestinal parasites infection, which suggests a possible soil-related transmission of intestinal parasites.

Intestinal parasites parasitize a wide range of mammalian hosts through zoonotic and anthroponomical means. The association observed between goats and STH has not been reported. The Trichuris spp. observed could be Trichuris ovis isolated in goat43 although T. ovis ova are slightly larger in diameter and are similar to T. trichiura in humans. It is important to control intestinal parasites in animals as a focused strategy of decreasing human infections. Further studies could also be done to investigate a possible link between soil-transmitted helminths and goat rearing.

Conclusion

In conclusion, the present study showed a low prevalence of intestinal parasitic infections among school-going children in an informal urban setting of Nakuru town. The low prevalence could be accounted for by improvements in water, sanitation, and hygiene (WASH) practices. The current WHO recommendation for national deworming programs in schools is prevalence above 20% as children are considered to be at risk of infection. The risk factors were associated with poverty and were more related to hygiene and sanitation status and hence if the overall hygiene is improved in informal settlements, they may not be needed for preventive chemotherapy. Contact with domestic animals and their waste also contributed to higher infections in this study. This suggests the need for regular deworming of animals and being kept away from humans as some could act as potential reservoirs to intestinal parasitic infections. As a limitation, the study did not factor in the possibility of the child having taken deworming tablets prior to the study.

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