Poverty, Dietary Intake, Intestinal Parasites, and Nutritional Status among School-Age Children in the Rural Philippines

Intestinal helminths are endemic throughout the Philippines; however, there is limited evidence with respect to their prevalence, intensity, and impact on children’s nutritional status. A cross-sectional survey was carried out on 693 children from five rural villages in Northern Samar, the Philippines. Data on dietary intake, nutritional status, and intestinal parasites were collected. Infection with Schistosoma japonicum, Ascaris lumbricoides, Trichuris trichiura, and hookworm was evident in 20.1, 54.4, 71.4, and 25.3% of the children. The majority (84.7%) was infected with one or more helminth species, with about one-quarter of the sample (24.7%) infected with three or more. About half (49.2%, n = 341) of the children were stunted and 27.8% (n = 193) were wasted. A lower prevalence of normal height-for-age (48.3%) appeared in those with polyparasitism, while the prevalence of stunted children increased with infection (46.7% monoparasitism and 51.7% polyparasitism). There was a decreasing trend between infection intensity and the mean values of HAZ and BAZ identified for T. trichiura or hookworm infections. Stunted children were more likely to be male (AOR = 1.58; 95% CI: 1.05–2.39; p = 0.028), older in age (10–14 years) (AOR = 1.93; 95% CI: 1.29–2.88; p = 0.001), and living in poorer households with palm leaves/nipa roof (AOR = 1.85; 95% CI: 1.14–3.01; p = 0.013). Intestinal parasitic treatment needs to be combined with nutrient supplements and health education in order to interrupt the parasite life cycle and achieve sustainable control.


Introduction
More than a third of the world's population is infected with soil-transmitted helminths (STH), mainly in the developing nations of Asia, Africa, and Latin America [1]. STHs are intestinal parasitic nematode worms causing human disease. They are the most common of the 17 major neglected tropical diseases (NTDs) and the most widespread and disabling chronic infections globally [2]. Ascaris lumbricoides is the most prevalent STH with an estimated one billion infections; and Trichuris trichiura and hookworms (Necator americanus and Ancylostoma duodenale) each infect approximately 600-800 million [1]. STHs are a significant public health concern in the Philippines, particularly among school-aged children who, if infected, suffer from profound physical deficits,

Study Procedures
Individuals were asked, over the course of a week, to provide two stool specimens from which six Kato-Katz thick smears were prepared on microscope slides. These slides were examined under a light microscope by experienced laboratory technicians who counted the number of STH and Schistosoma japonicum (SJ) eggs per slide. For quality control, 10% of slides were randomly selected and re-examined by a senior microscopist at the Research Institute for Tropical Medicine, Manila. Individual and head of household questionnaires were completed to collect the following information: occupation, level of education, home and land ownership, number of animals owned and raising practices, animal waste disposal practices, pasturing of animals, sanitation, and housing characteristics (roofing, wall, and floor materials). For wealth status, participants were classified as wealthy if their house had a cement floor, a galvanized roof, cement walls, and a tile/marble floor. Participants were classified as poor if they had a house with a nipa (palm) roof and a soil floor, and without cement walls. All other participants were classified as having a moderate wealth status.

Nutritional Assessment
Anthropometric measurements of height and weight were collected using standard procedures [23]. Weight was measured using a portable digital scale to the nearest 0.1 kg. Height was assessed to the nearest 0.1 cm using a tape measure. The Z values for weight-for-height (WAZ) (children aged <10 years only), body mass index (BMI)-for-age (BAZ), and height-for-age (HAZ) were calculated according to World Health Organization (WHO) guidelines using the new WHO growth standards [24,25]. Weight-for-height is considered an inappropriate indicator for monitoring child growth beyond the age of 10 due to its inability to distinguish between relative height and body mass. Therefore, BMI-for-age was used to assess thinness/wasting for children aged ≥10 and for adolescents. Based on the Z values, the children were categorized as 'thin/wasted' (BAZ < −2 and/or WAZ < −2) and 'stunted' (HAZ < −2). Children with Z values > −2 for BAZ, WAZ, and HAZ were categorized as 'normal'.

Dietary Intake Data
Dietary intake information was elicited using a 24-h recall method. Three qualified nutritionists together with 10 field nurses collected the data. Household food utensils were used to assist study participants quantify food portions and liquids consumed. In order to estimate food weights, macroand micronutrient intakes were calculated for each child using food composition tables developed by the Food and Nutrition Research Institute [26]. These tables contained data on 17 food components of 1541 foods commonly consumed in the Philippines. Dietary intake data was evaluated against the national Filipino recommended energy and nutrient intake (RENI) values by age and sex [27].

Statistical Analysis
Data were double-entered into FoxPro (version 6.0), crosschecked, and subsequently analysed using STATA SE version 13.0 software (StataCorp LP, College Station, TX, USA). All variables including sex, age group, and endemic setting were explored individually by Chi-square statistics. Infection intensity was explored with the Student t-test and Kruskal-Wallis test. The standard error (SE) of each estimate was converted to a variance; all variances were summed to provide an overall variance, SE, and 95% confidence interval (CI). The Chi-square test and the Student t-test were used to explore associations of a participant's demographic and socio-economic characteristics and the likelihood of having S. japonicum, any STH, and any helminth infection. Significant demographic and socio-economic factors were entered into the mixed-effect logistic regression analysis to obtain the final model for predicting stunting. Random barangay (village) and household effects were included in the model to account for the correlation among observations within each barangay and household, respectively. Adaptive Gaussian quadrature with 10 points was adopted to approximate the log likelihood for all levels of both random effects in the mixed model. Factors that were not significantly relevant (cut-off for significance = 0.05) were removed in a stepwise backward regression elimination procedure.

Study Oversight
Ethical consent for the study was obtained from the ethics review boards of the Department of Health in the Philippines (IRB # 2012-13-0) and Griffith University, Australia. Written informed consent was obtained from the parents/legal guardians. All questionnaires were translated into the local dialect and back-translated into English. Individuals found positive for a STH or S. japonicum were treated according to the Department of Health clinical guidelines.

Demographic, Household, and Nutritional Characteristics and Prevalence of Infection
A cross-sectional survey was carried out on 693 children, of whom 53% were male. A total of 41.7% of the study population was aged between 6-9 years with the remainder between 10-14 years. The majority of children (56%) lived in a house with a roof made from either palm leaves or nipa, an indirect indicator of lower socioeconomic status. Infection with S. japonicum, Ascaris lumbricoides, Trichuris trichiura, and hookworm was evident in 20.1, 54.4, 71.4, and 25.3% of the 667 children sampled for intestinal parasites. The majority of the children (84.7%) was infected with one or more helminth species, with about one-quarter of the study sample (24.7%) infected with three or more different worm species.
The demographic, household, and nutritional characteristics of the study sample are presented in Table 1. About half (49.2%, n = 341) of the study sample were stunted and 27.8% (n = 193) were thin. Both mean HAZ and BAZ scores were below world standard (−2.0 SD and −1.3 SD from world mean, respectively). SJ infection occurred more often for males (64.2%, p = 0.003) and higher age group (70.2%, p = 0.002). Children with S. japonicum infection also had lower BAZ scores (−1.603, p = 0.039). Children with any STH infection were more likely to be of higher age group (60.5%, p = 0.019) or living in houses with palm leaves/nipa roofs (57.5%, p = 0.040). There was no significant difference for the nutrition indicators between children with and without any STH infection. Age group and roof material were the only factors that differentiated the three children groups of non-infected, monoparasitism, and polyparasitism (proportion of polyparasitism was higher for the higher age group, p = 0.018, and for those with house roof materials of palm leaves or nipa, p = 0.021). Table 2 presents the demographic, household, and nutritional characteristics of the study sample, by intensity of infection. Significant results were found between negative, light, and moderate/heavy SJ infection. Males (p = 0.01) and older children (p = 0.009) were more likely to have S. japonicum infection. For A. lumbricoides infections, children in the household without toilets (p = 0.009) or without galvanized iron/cement roof (p <0.001) were more likely to have moderate or heavy infections. These factors have the same impact for T. trichiura infections. Children in households without toilets (p < 0.001) or galvanized iron/cement roof (p = 0.038) were more likely to have moderate or heavy infections. Moreover, children with moderate or heavy T. trichiura infections had a significantly higher mean levels of vitamin C intake, compared to those with light infections (p = 0.038). Finally, children with light hookworm infections were more likely to be male (62.1% versus 49.4%, p = 0.004), to be stunted (61.5% versus 44.8%, p < 0.001), and had a higher proportion of households without toilets (25.7% versus 17.9%, p = 0.028), and lower mean HAZ Z-scores (−2.14 versus −1.92, p = 0.014) and BAZ Z-scores (−1.61 versus −1.37, p = 0.013).  Data are count (%) for categorical variables and mean (standard deviation) for continuous variables. a Significant difference between negative, light, and moderate/heavy SJ infection in gender (p = 0.01) and age group (p = 0.009). b Significant difference between negative, light, and moderate/heavy A. lumbricoides infection in the proportions of owning toilet (p = 0.009) and galvanized iron/cement roof material (p < 0.001). c Significant difference between negative, light, and moderate/heavy T. trichiura infection in the proportions of owning toilet (p < 0.001) and galvanized iron/cement roof material (p = 0.028), and the mean level of vitamin C (p = 0.038). d Significant difference between negative and light hookworms infection in gender (p = 0.004), the proportions of owning toilet (p = 0.028) and stunted children (p < 0.001), and the mean levels of the HAZ Z-score (p = 0.014) and the BAZ Z-score (p = 0.013).

Demographic, Household, and Nutritional Characteristics and Intensity of Infection
As depicted in Figure 1, a decreasing trend between infection intensity and the mean values of HAZ and BAZ was identified for T. trichiura or hookworm infections (that is, the heavier the intensity, the lower the HAZ and BAZ mean values). For SJ or A. lumbricoides infections, the trend was not so obvious.
As depicted in Figure 1, a decreasing trend between infection intensity and the mean values of HAZ and BAZ was identified for T. trichiura or hookworm infections (that is, the heavier the intensity, the lower the HAZ and BAZ mean values). For SJ or A. lumbricoides infections, the trend was not so obvious.  Table 3 displays the mixed-effect logistic regression model for stunting. Compared to children with normal height for age, stunted children were more likely to be male (AOR = 1.58; 95% CI: 1.05-2.39; p = 0.028), older in the age group of 10-14 (AOR = 1.93; 95% CI: 1.29-2.88; p = 0.001), and living in poorer households with palm leaves/nipa roofs (AOR = 1.85; 95% CI: 1.14-3.01; p = 0.013). All nutrition factors were not significantly associated with stunting. Variation among the predicted barangay-specific random effects for stunting was not statistically significant. However, there is significant household-specific random effects (estimated variance: 1.82, p < 0.001) in the probability of stunting, indicating that unknown household effects other than the identified household risk factor (roof materials) exist.  Table 3 displays the mixed-effect logistic regression model for stunting. Compared to children with normal height for age, stunted children were more likely to be male (AOR = 1.58; 95% CI: 1.05-2.39; p = 0.028), older in the age group of 10-14 (AOR = 1.93; 95% CI: 1.29-2.88; p = 0.001), and living in poorer households with palm leaves/nipa roofs (AOR = 1.85; 95% CI: 1.14-3.01; p = 0.013). All nutrition factors were not significantly associated with stunting. Variation among the predicted barangay-specific random effects for stunting was not statistically significant. However, there is significant household-specific random effects (estimated variance: 1.82, p < 0.001) in the probability of stunting, indicating that unknown household effects other than the identified household risk factor (roof materials) exist.

Discussion
The current WHO strategy for intestinal helminths in children is to continually treat pre-school and school-age children at high risk once or twice per year depending on prevalence [8]. This is effective in achieving morbidity control; however, it does not prevent re-infection. Our study area has participated in national control efforts for over two decades yet the prevalence of helminth infection remains stubbornly high due largely to poverty and malnutrition. In our study, we found that approximately 85% of the rural children were infected with one or more helminth infections. T. trichiura infections (71.4%) were found to be more prevalent than A. lumbricoides (54.4%) infections. Moreover, about half (49%) of the study sample were stunted and almost a third (28%) were wasted. Stunted children were more likely to be male, older in age (10-14 years), and living in poorer households with palm leaves/nipa roofs.
In the mixed-effect logistic regression model for stunting all of the nutrition factors (i.e., grams) were found not to be significantly associated with stunting. However, we previously found a significant association between the coinfection of all four helminthiases and low intakes of energy, thiamine, and riboflavin among children, when the recommended energy and nutrient intake (RENI) for total calories was examined [21]. Thiamine and riboflavin deficiencies are common in Northern Samar, where dairy and meat intakes are low and mostly rice-based meals are consumed [21]. Iron deficiency has been associated with impairments in both adaptive and innate immunity and with lowering the body's resistance to infectious diseases [21]. Poor nutrient intake may increase susceptibility to parasitic diseases and together they negatively affect the nutritional status of children and adolescents [21].
We believe that a deworming program must be coupled with a nutrition program at the primary school level. Children are presently eating 1-2 meals per day at home and this is insufficient to meet their macro or micronutrient requirements. An additional meal at school appears to be of paramount importance for those severely malnourished. In order to address this problem the Philippine government has initiated the school-based feeding program called 'Gulayan sa Paaralan', which has been successfully piloted in approximately one percent of schools. However, to date it has not been formally evaluated in a clinical trial.
An appropriate eight-week micronutrient weaning period of 'ready-to-use therapeutic foods' (RUTF), with demonstrated immune-modulating functions-including iron, zinc, calcium, vitamin A, B and C, n-3 and n-6 fatty acids-also needs to be considered following the macronutrient school intervention. In a recent pilot study conducted at the Philippine General Hospital, the researchers created their modified version of RUTF from commercially-available ingredients including milk, sugar, coconut oil, and peanut butter [28]. A total of 100 children (aged 18 months to 10 years) was randomized to either a RUTF group, who received the supplement, and a control group, who did not [28]. The treatment group received RUTF on weekdays for five weeks. Changes in weight, height, and arm circumference were recorded for five weeks and two weeks after supplementation. Results of the study showed that RUTF was an effective, safe, and acceptable alternative supplement for children with mild to severe malnutrition [28].
Annual or biannual albendazole treatment (i.e., 400 mg) needs to be combined with macro/micronutrient supplements, WASH, and health education in order to interrupt the life cycles of STH diseases, prevent reinfection, and achieve sustainable control. A well-nourished population, with an intact immune system, has a better chance of warding off future parasitic infection. Simply providing drugs to malnourished populations, which is a common practice in the global control of STHs, is not the answer. Both poverty and malnutrition must be addressed if future MDA programs for NTDs are to have a lasting impact.