The fundamental basis of the relationship between an infectious organism and its host is basically nutritional because the host is the source of all nutrients needed by the organism for maintenance, growth, and reproduction.104The combination of a high prevalence of STHs and poor hygiene and malnutrition is an indicator of a country’s future problem. Therefore, the eradication of STHs worldwide should be given a high priority.153This study was carried out to assess the prevalence of STH, the nutritional status and the prevalence of anaemia in pupils of rural and urban areas of Lagos State.
Characteristics of respondents and their parents
A higher proportion (54.7%) of respondents overall were ten years and older. There were more pupils that were ten years and above (60.6%) in the rural area. The same pattern was found in Kwara state in a study assessing intestinal helminthes among pupils rural and urban communities where there were older children and in Ozubulu, Anambra state where 58.1% of the pupils examined were more than ten years old.58, 294 Also in Wakiso district in Uganda where 78.5% of the pupils were ten years and above.115 The age group proportion was almost the same in the urban area but more pupils (51.1%) were in the six to nine years age group. The mean age was also significantly higher in the rural area. The reason for this might be due to late school enrolment in the rural area because it is assumed that less literate people are in the rural area hence the importance of educating their children might not be given topmost priority.
Also, delayed physical growth caused by undernutrition might cause delay in school enrolment in the rural area since they have lower socio – economic status. The sex distribution showed that overall, there were more females (54.2%). In the rural area, 59.5% of the respondents were
165 females but in the urban area, there were slightly more males (51.1%).The same pattern was found in a study assessing the impact of intestinal parasitic infections on the nutritional status of rural and urban school-aged children in Akwa Ibom State, where there were more females in the rural and more males in the urban.295 In studies conducted in Kwara State and Wakiso district, Uganda, 54.6% and 51.9% of the pupils were females.58,115 This is, however contrary to a study in Ikenne where 56.8% were boys and 43.2% were girls.51 The NDHS 2008 of Nigeria also revealed that net attendance ratio in primary school was 59.1% females and 64.9% males.194
Most of the respondents (86.4%) from both locations indicated that their mothers were married, 83.7% from rural area and 89.0% from urban area. and most (83.4%) were also in monogamous marriages, almost equal proportion in rural (83.7%) and urban (89.0%) areas.
About half (50.8%) of the total respondents’ mothers had primary and no formal education, being higher in the rural area (64.0%) compared to the urban (37.5%) This difference found to be statistically significant (p <0.001) is comparable to a similar study in Kwara state.58 The educational level of the respondents’ fathers showed that a lower proportion (34.8%) had primary and no formal education. The occupation of the respondents’ parents indicated that majority of them (mother and father) were in the middle occupational class.
Hygienic and environmental conditions of the respondents showed that 57.2% of the respondents had shoes on after school when playing outside their houses with more of them in the rural (63.6%) than the urban (50.8%). This is against what would have been expected but urbanization could cause this as was found in a Malawian study where there was a higher risk of infection in the urban area and one of the risk factors after controlling for confounders was not wearing shoes (OR= 7.1; CI = 2.7-19.2) among others.296
166 Prevalence and intensity of Soil-transmitted helminthiases
In this study, the cumulative prevalence of STH in both locations was 33.3%.This is comparable to recent study in Ife central LGA, Osun state where a prevalence of 30% was obtained.60 Also in congruence with that obtained in Adama, Ethiopia among first-cycle primary schoolchildren (35.5%).218It is higher than some recent studies in Kwara state and Ugandan school children with cumulative prevalence rate of 17. 6% and 16% respectively;
58,115 though still lower than those obtained from two similar studies in Ogun state with cumulative prevalence rates of 50% and 66.2% and another in Akwa Ibom state with prevalence of 67.4%.51, 59, 295 There was a higher prevalence of 41.5% in the rural area compared to 25.2% in the urban area, ( p < 0.05 ). The rural area prevalence is in congruence with a recent study in four rural areas of Kwara state where a prevalence of 41.9% was obtained.297 It is closer to that found in studies in primary school pupils in Ozubulu, Anambra State and rural Malay children with prevalences of 48.08% and 37% respectively.294, 298It is lower than findings from other studies conducted in rural of Ikenne and Ondo State,51,54 but higher than findings from some other recent studies in Kwara State, South western Nigeria and Southern Malawi 58, 60,296 The urban prevalence of 25.2% is also in congruence with a study at Ife where a prevalence of 24.3% was obtained in the urban area.60 It is higher than what was obtained from several other studies in Onicha, Kwara State and Southern Malawi,53,58, 296 but lower than results from studies at Ikenne and Ilorin with prevalences of 54.9% and 47.4%
respectively.51,56 The statistically significant difference between the two locations with a higher prevalence in the rural area is consistent with that of previous studies at Ikenne, Ife and Akwa Ibom State.51,60,295 but not consistent with some others where no statistically significant differences were found in STH prevalence between rural and urban areas like that of Kwara State and Malaysia .58,61 It also contradicts a similar study where prevalence of helminth infection was significantly higher in the urban subjects than in the rural (16.5% v. 3.6%; P<
167 0.001) amongst Malawian children.296 The co-infection prevalence was also higher in the rural than in the urban area and this is similar to the finding reported at Ikenne where multiple infections were higher in the rural government school than in the urban government school.51 The higher prevalence of STH in the rural area is not surprising since the rural areas were worse in their hygienic and environmental conditions and also had respondents whose parents’
socio – economic characteristics were worse when compared with the urban area and these factors amongst others have been found to perpetuate the continued existence of STHs. There was also indiscriminate defecation in the school compounds and bushes around the school because the toilet facilities were not enough for the number of pupils available; hence, part of the reasons for the poor conditions of these facilities.
Ascaris lumbricoides was the most prevalent helminth with a rate of 24. 6% overall and 27.4%
and 21.9% in the rural and urban area respectively, though the difference was not statistically significant. This is consistent with several recent studies where Ascaris lumbricoides has also been found as the most prevalent helminth among school children like that of Ikenne,51 Kwara State,58 Ogun State,59 Osun State, 68 and Uganda.115 The highest prevalence of A. lumbricoides recorded in this study could indicate high level of unhygienic practices and the habit of defaecating indiscriminately in open place among school children which eventually contaminate the environment. Also, it is well established that the infective stages of A.
lumbricoides, the embryonated eggs have enormous capacity for withstanding the extremes of temperatures.299 Therefore, they could be kept alive for a longer period than the other STHs.
Most (87.6%) of the respondents had light intensity overall and higher proportions of Ascaris and Trichuris infection and all of hookworm infection were light intensity infection. There were no statistical significant differences ( p > 0.05 ) in the intensity of STH between rural and urban areas and this is in congruence with several recent studies like that among Ugandan
168 children where it was found that none of the children investigated had a moderate to heavy form of infection.115 In East Guatemalan peri urban/rural school children (Izabal province), most as of the infection was low-intensity infection.300 The low intensity infection obtained could be attributed to the school de-worming programme that is on in Lagos State, thus the reduction in the prevalence and intensity of the helminth infections. There was no statistically significant difference ( p> 0.05) in the mean egg per gram of Ascaris lumbricoides between rural and urban area and this is consistent with a similar studies in Ogun State,59 but the differences in the mean epg of Trichuris trichiura and Hookworm between rural and urban areas were statistically significant. Other studies have found statistically significant differences (p<0.05) in the mean eggs per gram of STH between urban and rural areas like that of Kwara State and Ogun State.58, 59 and in a similar study at Ife, the mean intensities of Ascaris infection were significantly lower among the infected rural children than among the infected urban. 60
Nutritional status of children
The overall prevalence of undernutrition was 11.6% .This prevalence is lower than that from a cross sectional study conducted in schools of Kaski district of Western Nepal with a prevalence of 26%.188 but higher than the prevalence in school children in Peru where a co-prevalence of underweight and stunting was 9.3%.179 There was a higher prevalence of 17.8% in the rural compared with 5.3% in the urban area and this difference was statistically significant (p = 0.000). The prevalence of stunting in this study was 11.4% overall with a higher prevalence of 18.2% in the rural area and 4.5% in the urban area. This is in congruence with a similar study in Jos among newly enrolled school children where the prevalence of stunting was found to be 11.1%. 191 It is lower than that reported among school children in Uganda, Lagos State, Makurdi and Osun State with prevalent rates of 22.5%, 40.5%, 52.7%, and 26.7% respectively.
115, 189, 190, 192 Higher prevalence of stunting in the rural area compared to urban area is
169 consistent with a similar study in Akwa Ibom where 42.3% pupils in rural compared to 29.7%
pupils in urban were stunted,295 and also in Ouagadougou, Burkina Faso where the prevalence of stunting in the peri urban school children was higher than that in the urban school children ( 16.0% versus 7.4% ).301 It is however, inconsistent with a similar study among urban and rural slum school children in Uganda where children in urban slum schools were 1.7 times more stunted compared to those rural (p = 0.027).115 The prevalence of thinness in both locations according to WHO Reference 2007 was 10.0% with a higher prevalence of 13.6% in the rural and 6.4% in the urban. It is higher than the prevalence among adolescents in Ahmedabad, India 193 and all the prevalent rates were lower than the ones obtained from recent studies like that in Makurdi (77.3% ), Umuahia (24.2% in boys and 19.2% in girls), Northern Ghana (29.8%) and Bengal, India (6 2.9% in boys and 61.% in girls ).190,302,303,304 Underweight in the six to nine year age group was 11.4% in both locations with a higher prevalence of 20.4% in the rural and 3.5% in the urban. The overall prevalence is similar to that found in studies in Peru and Jos with prevalence rates of 10.5% and 10.3% respectively.179,191 The rural prevalence is in congruence with that obtained from a study in rural Osun state with underweight prevalence of 23.1%,192 but the prevalence gotten from this study is lower than that from several other studies,14,189,190,246,295,299 and higher than few other ones like that among children in Wakiso district in Central Uganda with a prevalence of 5.3%.115 One explanation for the lower prevalence of undernutrition in this study could be the lower helminth infection prevalence and intensity of infection compared to settings where both prevalence and intensity of helminth and stunting levels were high. Moderate-to-heavy intensity helminth infections have been reported to be a risk factor for the high stunting prevalence among school children.305 It could also be due to the routine de-worming programme on going in Lagos State.
The better nutritional status of children in urban area in this study agrees with findings in other studies in Nigeria, 306,307and other developing countries like South Africa and Angola.308,309
170 The difference might also be due to the lower educational status of the rural parents. Both female and male education can have a positive effect on the child’s nutritional status.
Knowledge can lead to a higher household income and better nutritional status when the education is linked with strategies to improve both.199
In addition, urban mothers were engaged in better paying occupations, thus resulting to better nutrition in their children. Also, it is possible that due to urban- rural migration, there are less people left in the rural areas to farm and produce food, as many have drifted to the urban area in search of greener pastures.
Prevalence of anaemia
The study revealed that the prevalence of anaemia was 19.0 % in both locations with a higher prevalence of 21.3% in the rural and 16.7% in the urban though no statistically significant difference between both locations. It is slightly higher than what was found in Bangalore district in India (13. 6%) where no statistically significant difference was observed between rural and urban areas.242 In rural China among school aged children, the prevalence of anaemia was 13.1%.305 In Ouagadougou, Burkina Faso, the prevalence in the urban area was even higher than in the peri - urban area ( 40.7% versus 38.7% ), though the difference was not statistically significant too.301 Otherwise, the prevalence of anaemia from this study is lower than most previous studies in Nigeria like 38. 6% in rural Ovia North East LGA of Edo State and even much higher rates such as 87.1% in Odogbolu and 82.6% in rural communities of Abia State among similar study population.247,248 The reason for the lower prevalence rate of anaemia in this study compared to some recent studies in Nigeria might be because of the low prevalence and intensity of STH especially hookworm and Trichuris infections since the amount of blood loss in hookworm infections is strongly and linearly correlated with worm
171 load and faecal egg count,32 and Trichuris trichiura also causes intestinal blood loss. All the hookworm infections found in the study were light intensity infections in both locations.
Co - Prevalence of STH, Undernutrition and Anaemia.
The prevalence of STH, undernutrition and anaemia from this study revealed that small proportion of the participants had a combination of either two or the three, the highest prevalence being 5.3% for subjects with both STH and anaemia and the least prevalence being 0.9% for those who had the three. There was a statistically significant difference (0.004) between rural and urban areas among those with STH and undernutrition; overall prevalence being 4.0% with 6.4% rural prevalence and 1.5% urban prevalence. This is in congruence with a similar study at Uganda where 5.1% of the pupils were infected and stunted and 1. 65% of the pupils were infected and underweight,115 but theseprevalence rates are much lower than that obtained from a recent study among school aged pupils in two rural areas in China where the co prevalence of anaemia and stunting was 40.7%.305
Risk factors of prevalence and intensity of Soil-transmitted helminth infection.
It was obtained from this study that urban area pupils were less likely to be infected with cumulative soil- transmitted helminths than pupils in the rural area. This pattern was also found with Trichuris and Hookworm infections but not with Ascaris infection. This is consistent with findings from similar studies like that of Ikenne and Akwa Ibom State in Nigeria.51, 295 In Uganda, children who attended rural primary schools were 1.95 times more likely to be infected compared to those in the urban slum schools (p= 0.012).115 The reasons for this finding might be quite obvious being the preponderance of those factors that predisposes to acquiring these infections are more in the rural areas than the urban areas especially the environmental factors. It contradicts what was found in few other studies, for example, the mean intensities of Ascaris infection were significantly lower among infected rural children than among the
172 infected urban in Ife.60. Also, in Malawi living in an urban community was associated with a significantly higher risk of infection even after controlling for potential confounding factors (OR = 5.3; 95% CI= 2.6-12.1).296
The other risk factors found to be statistically significantly associated with prevalence of STH on bivariate analysis were pit latrine use with Ascaris lumbricoides infection (P = 0.031) in the urban area and pit latrine use and indiscriminate defecation with Trichuris trichiura infection ( P = 0.010 ) in the rural area. Also, the sex distribution was statistically significantly associated with Trichuris trichiura infection, a higher proportion of female pupils being more infected (P
= 0.035) in the urban area. After multivariate analysis using logistic regression, the other predictors of STH were pit latrine use (OR = 1.69; 95% CI = 1.01 – 2.83; P –value = 0.045) and the other type of toilet facility being used by the respondents like open defeacation, defaecating in the bush and digging the ground to defeacate (OR = 1.96; 95% confidence CI = 1.09 – 3.55; P –value = 0.026) for cumulative STH infections, pit latrine use for Ascaris lumbricoides infection [odds ratio (OR) = 1.86; 95% confidence interval(CI) = 1.09 – 3.18; P – value = 0.023] and open defeacation and defaecating in the bush for Trichuris trichiura infection (OR = 2.37; 95% CI = 1.06 – 5.33; P –value = 0.03). These findings are consistent with those of recent similar studies like the cross sectional study among pupils in Umuebe community of Delta State where multiple logistic analysis for the epidemiological variable revealed the use of pit latrine [odds ratio (OR) = 1. 66; 95% confidence interval(CI) = 1.34 – 3.96; P –value = 0.041] and bush/no toilet (OR= 29.24; 95% CI= 12.58 –67.95; P –value = <
0.001) compared to water closet as a logistic risk factor ( predictor ) for A. lumbricoides and bush/no toilet (OR = 0.19; 95% CI = 0.06 – 0.59; P –value = 0.004) as a logistic risk factor for Trichuris trichiura infection .310 Also in Kwara State in a similar study, the female pupils had a relatively higher prevalence rate than males and the use of pit latrine was associated with a lower risk of acquisition of intestinal helminth compared to the use of open bush.58 In
173 Ozubulu,Anambra State, females had the highest STH prevalence rate of 76 (55.47%) compared to the males with the rate of 49 (39.84%) and this was statistically significant (P<0.05).294 In Enugu, sites utilized for defeacation by the pupils significantly influenced the rate of helminthic infection. ( p = 0.001).311 Itis also consistent with a recent prospective study conducted among rural and urban school children of Kashmir in India where parasitoses was significant higher in those children who would go for open defeacation compared to those children who used flushed and pit ( P < 0.05 ).312 The probable explanation for the female sex having higher prevalence in this study might be that they are more exposed to potential domestic sources of transmission of these helminths, like food preparation, fetching water, and disposal of waste than their male counterpart and the reason for higher prevalence with open defeacation and pit latrine use when compared to water closet in this study might be that with water closet use, there’s reduction of contact between persons and the infective larvae. In Delta State however, the sex related prevalence showed that males were more infected for all species of STHs than females.310 Younger children (six to nine years old) were found to have Trichuris infection more than the older children in both rural and urban area but the prevalence of hookworm infection was higher among the older age group ( ≥ 10 years of age ) though these differences were not statistically significant ( P > 0.05 ). This is in congruence with similar studies like that found in a rural community where prevalence was highest among children aged 12 – 17 years (81.6%) compared to 63.3% and 52.4% in those aged 6 – 11 years and 0 – 5 years respectively.52 In Kwara State, children > 12 years had a higher prevalence of STHs.58 In Enugu among nursery and primary school children, prevalence of hookworm and Ascaris increased with increase in age,294 and in Umuebu Community of Delta State, multiple logistic regression showed the prevalence and intensity of all species of STHs to significantly vary with age with the highest prevalence in age group 5 – 7 years.311 Among elementary school children of Zarima town in Northwest Ethiopia, age group 5-9 years showed statistical
174 significant association with STHs compared to other categories.109 Hookworm infections were more prevalent among those 12 years of age or older (OR 2.9; 95% CI 1.2-7.1) in a village survey in rural South-West China.112 Though not statistically significantly associated with helminthic infection ( P > 0.05 ), children whose mothers’ educational level was primary education in the rural area had a higher prevalence of STH while those with tertiary maternal education in the urban area had a higher prevalence. In a similar study in Kwara state of mothers who had higher education had a higher prevalence of STHs.58 In China, children of mothers with educational attainment of secondary school or higher had a protective effect against T. trichiura (OR 0.18; 95% CI 0.06-0.54) and hookworm (OR 0.21; 95% CI 0.09-0.51) infections.112 On the other hand among rural Malay children, poor education of the mother (primary education or less) (P=0.015) were found independent risk factors for the child's helminth infections in univariate analysis and in a multivariate analysis of predictors of helminth infection, poor education of the mother (P=0.02) remained statistically significant, after controlling for several other potential risk factors.300 The reason for the higher prevalence in respondents with low maternal education in the rural area is not far-fetched since the hygienic practice of their mothers and care generally might be affected by their low educational level. The higher prevalence in the children of mother’s with higher educational level in the urban might be explained by the same reason as that of the Kwara State study which is that due to the increasing number of women in the workforce, children are left with no choice but to patronize food vendors.313
Father’s occupationconsidered as the index of family income and wealth in this study showed that has also been found to be associated with prevalence of STHs. A higher proportion of respondents whose father’s occupation was low class had STH though this association had no statistical significance. This was also observed in Enugu where infection occurred most in pupils whose parents were farmers (an index used as poverty level in the study).294 Also,
175 Tanzanian participants belonging to the least poor wealth quintile were at a significantly lower risk of a T. trichiura infection than their counterparts belonging to the most poor wealth quintile (OR = 0.28, 95% CI 0.10–0.82) in a similar study.110. This can be explained by the fact that they have a lower income and therefore low purchasing power resulting in low availability of food. Walking barefoot has also been found to be a risk factor for STH especially hookworm infection as evidenced by findings from several studies like that of Delta State where after multiple logistic regression, walking barefoot was a risk factor for hookworm.309 Also in Enugu, the rate of helminthic infection varied significantly with the use of footwear after school hours (p=0.001).311 The finding from this study did not reveal this. Anotherhygienic factor that has been found in studies is hand washing habit after defeacation and from this study, there was a higher prevalence of cumulative STH and Trichuris infection among those who did not wash hands after defeacation and if they did who used only water and other substances like ashes and leaves to clean their hand when compared to those who washed with soap and water. This is in congruence with studies like that carried out in Ethiopia.109 Also in peri-urban area of Zanzibar, Tanzania, washing hands after defecation was determined as a protective factor against a T. trichiura infection (OR = 0.06, 95% CI 0.01–0.26),110 and in the cross sectional survey of children attending nursery and primary schools in Enugu, the rate of helminthic infection varied significantly with hand washing habits after defeacation
(P= 0.001).311 The source of drinking water is another factor that was considered and though no statistical significant association was found between it and rate of helminthic infection in this study, there was a higher prevalence of infection in respondents who drank from well and other unknown sources like buying water from cart pushers and sachet water compared with those who drank pipe borne and bottled water in both locations. Findings like that were obtained from several similar studies like the study at Majidun and Owutu Sub- Urban community of Lagos where provision of water was a stronger determinant of lower intestinal parasitic
176 prevalence.95 In Umuebu Community, Delta State, result from multiple regression revealed drinking from well or surface tanks was risk factor for A.lumbricoides and T.trichiura, 310 and also, the rate of helminthic infection varied significantly with the source of drinking water ( P = 0.01 ).311
The mean intensities of Trichuris infection and Hookworm infection were statistically
significantly higher in the rural than the urban area but there was no statistically significant difference in the mean intensities of Ascaris infection between the rural and the
urban. This is contrary to the findings at Ife where the mean intensities of Ascaris infection were significantly lower among infected rural children than among the infected urban in Ife.60 The type of toilet facility used in the rural area by the respondents was found to be statistically significantly associated with moderate intensity of STH (p=0.008), being higher amongst those that used pit latrine (31.6 %) and after multiple logistic regression, younger age group (6 – 9 years (OR = 3.2; 95% CI= 1.5-8.7; P – value = 0.026) and the use of pit latrine (OR = 2.9;
95% CI= 1.0-8.2; P – value = 0.045) were found to be predictors of moderate intensity of STH.
This is in congruence with a study in South Indian fishing village where the intensity of A.
lumbricoides infection was higher among younger children than older children, also identified with multivariate analysis.
Risk factors of Undernutrition (thinness and stunting) and anaemia
It was obtained from this study that urban area pupils were less likely to be thinned compared to their counterparts in the rural area (OR = 0.43; 95% CI = 0.23 -0. 79; P-value = 0.007). This trend was also found with stunting (OR = 0.22; 95% CI = 0.11 -0. 44; P-value = < 0.001). This has been found in similar studies as explained above and the reasons for these disparities have also been explained above. In both location, the prevalence of stunting increased with age and even after multiple logistic regression, the younger children were less likely to be stunted than
177 the older (OR = 0.23; 95% CI = 0.11 -0. 47; P-value = <0.001).This is in congruence with findings from some studies in Nigeria.306,314 Also in Uganda, children in the age group of 10–14 years old were 2.9 times more likely to be stunted compared to the other age group (P = 0.002),115 and in Kuala Lumpur.315 This may not be unconnected with deterioration in the socio-economic situation in the country, which has led to families concentrating meagre resources to catering for the youngest member of the families, to the detriment of the older children who need the nutritional support as they become adolescents in preparation for adulthood. Also, the extra demands that come as children grow (like increased play or walking long distances to school) create a need for energy that is much greater than that of pre-school and early-school goers.
Stunting is an indicator of chronic malnutrition. Male pupils had a higher prevalence of stunting in both locations and higher prevalence of thinness in the rural area and after multiple logistic regression, female pupils were still less likely to be thin and stunted though this was not statistically significant. In Ogun State, boys were more malnourished compared to girls (P
= 0.002). 316 In Southern Nigeria more females (3.7%) than males (1.8%) were obese (p <0 .05). 301 As much as 24.2% of the boys and 19.2% of the girls were thin, based on the WHO standards, whereas, 17.3% of the boys and 15.5% of the girls were thin based on the IS standard in Umuahia.302 Also in other developing countries like in Tamale, Ghana, more boys than girls were found to be thin (38.5% vs. 23.6%, p=0.0241),303 same in Uganda,115 and in India, the overall (age-combined) prevalence of thinness was 62.9% and 61.6% in boys and girls, respectively.304 The reverse is however the case in developed economies were boys are reportedly more overweight or obese than girls as found in Canada and Europe.317, 318 The explanation for boys having a higher prevalence of undernutrition compared to girls as found in this study may be because boys especially in the rural areas help with the difficult tasks especially at home and in the farm and these tasks require physical exertion. Also, another