Epidemiology of infectious and non-communicable diseases and effect of health interventions on children’s physical fitness in Port Elizabeth, South Africa

Abstract

Background: Globally, more than 1 billion people are infected with soil-transmitted helminths (STHs; Ascaris lumbricoides, hookworm and Trichuris trichiura) and Schistosoma spp., particularly school-aged children in low- and middle-income countries (LMICs). The symptoms most frequently associated with these parasitic worm infections include abdominal pain, (bloody) diarrhoea, anaemia, growth retardation and cognitive impairment. As traditional lifestyle and diets change with social and economic development, disadvantaged communities in LMICs increasingly also face non-communicable diseases. Particularly in urban settings, obesity-related conditions impose a growing burden and affect people from all socioeconomic strata. Together, this results in a double burden while health systems weaken in many countries, partially explained by high rates of urbanization in face of inadequate infrastructure development. This puts children at an increased risk of compromised health that may hamper their development, wellbeing and socioeconomic future.

Goal and specific objectives: The ‘Disease, Activity and Schoolchildren’s Health’ (DASH) study, a cluster-randomized controlled trial carried out in Port Elizabeth, South Africa, aimed to investigate the relationship between physical fitness and infections with STHs, intestinal protozoa and Helicobacter pylori among Grade 4 schoolchildren in quintile 3 primary schools through two 10-week multidimensional school-based physical activity interventions. The specific objectives of this study were (i) to determine the prevalence of intestinal parasite infections and H. pylori; (ii) to assess the haemoglobin (Hb) levels and anthropometric indicators; (iii) to comprehensively measure the physical fitness levels; and (iv) to investigate possible associations between infection status and socioeconomic status, self-reported physical activity score, and stunting. Based on the results, we developed a multidimensional intervention programme and assessed its effects on children’s cardiorespiratory fitness, body mass index (BMI) and thickness of skinfolds.

Research partnership and funding: The DASH study was a joint research endeavour involving colleagues from three institutions in two countries, (i) the Nelson Mandela University (Department of Human Movement Science, NMU) in South Africa, (ii) the Swiss Tropical and Public Health Institute, and (iii) the Department of Sport, Exercise and Health (Department of Sport, Exercise and Health, DSBG) of the University of Basel in Switzerland. Stool samples were analyzed in the laboratories of the Department of Medical Laboratory Sciences at the NMU with the support of Biomedical Technology (BTech) 4th year students. The study was funded by the Swiss National Science Foundation and the National Research Foundation in South Africa, as part of the Swiss-South Africa bilateral programme and the joint research project funding scheme.

Methods: This cluster-randomized controlled trial was implemented in 26 Grade 4 classes in eight disadvantaged primary schools in Port Elizabeth, South Africa. The selection of the study schools was based on their classification (quintile 3), the size of the Grade 4 classes (at least 100 children), geographical location and population demographics (Xhosa-, Afrikaans- and English-speaking children). The study was conducted in historically black and coloured (mixed race) government primary schools from various areas in Port Elizabeth in the south-eastern part of South Africa. The areas populated by black Africans are commonly referred to as townships and include the areas of Kwazakhele, New Brighton, Zwide and Motherwell. The ‘Northern areas’ in Port Elizabeth are largely made up of coloured people who were forcefully relocated from the central areas of the city to the outlying northern areas, and include the areas of Schauderville, Gelvandale, Helenvale, Hillcrest and Booysens Park. Fieldwork started in February 2015 (baseline). The midline assessment started in October 2015 and the endline was completed in May 2016. The first stage of the study included 1,009 children aged 9-12 years. Physical fitness was determined using field-deployable tests of the Eurofit fitness test battery. Stool samples were analysed with the Kato-Katz thick smear technique to diagnose STHs, and with rapid diagnostic tests (RDTs) to detect intestinal protozoa and H. pylori infections. Hb levels and anthropometric indicators were measured using standard tools and protocols. Demographic data and the socioeconomic status of each participant were captured with a questionnaire. Following the diagnosis of STH infections, children were treated with albendazole (single dose, 400 mg) after each survey. Our multidimensional physical activity intervention programme consisted of (i) physical education lessons twice a week; (ii) weekly dancing-to-music classes; (iii) in-class activity breaks; and (iv) school infrastructure adaptations to promote physical activity. Interventions were implemented twice, each time lasting 10 weeks. Additionally, the school feeding programme was reviewed with an aim to offering more balanced and nutritious food. Primary outcomes included cardiorespiratory fitness indicators measured by a 20 m shuttle run, BMI and thickness of skinfolds. Explanatory variables were socioeconomic status, self-reported physical activity, stunting, anaemia, intestinal protozoa and STH infection.

Results: Complete data at baseline were available for 934 children (92%). In two schools, high prevalence of STH infections were found (A. lumbricoides 60% and 72%, respectively; T. trichiura 65% each). For boys and girls co-infected with A. lumbricoides and T. trichiura (n=155) the maximal oxygen uptake (VO2 max) was estimated to be 50.1 ml kg-1 min-1 and 47.2 ml g-1 min-1, respectively, while it was 51.5 ml kg-1 min-1 and 47.4 ml kg-1 min-1 for their non-infected peers (n=278). On average, children without helminth infections had greater body mass (P=0.011), height (P=0.009) and a higher BMI (P=0.024) and were less often stunted (P=0.006), but not significantly less wasted compared to their peers with a single or dual species infection. Among 9-year-old boys, a negative correlation between helminth infections and VO2 max, grip strength and standing broad jump distance was observed (P=0.038). The overall mean Hb level was 122.2 g l-1. In the two schools with the highest prevalence of STHs, the Hb means were 119.7 g l-1 and 120.5 g l-1, respectively.

Across the three measurements, the mean A. lumbricoides infection intensities were 9,554 eggs per gram of stool (EPG) in May 2015, 4,317 EPG in October 2015 and 1,684 EPG in May 2016. The corresponding mean feacal egg counts for T. trichiura were 664 EPG, 331 EPG and 87 EPG. Results from a sub-study conducted in the two project schools with the highest STH prevalence showed that while albendazole was highly efficacious against A. lumbricoides (cure rate (CR): 97.2%; egg reduction rate (ERR): 94.5%), it lacked efficacy against T. trichiura (CR: 1.1%; ERR: 46.0%).

With respect to the effect of the multidimensional physical activity intervention programme on BMI, skinfolds and fitness, complete baseline and endline data are available from 579 children (mean age at baseline: 10.0 years). In the intervention group, we observed a significantly lower increase in the mean BMI (estimate of mean change: -0.12 with 95% confidence interval (CI): -0.22 to -0.03; P=0.008) and a reduced increase in the mean thickness of skinfolds (mean change: -1.06; 95% CI: -1.83 to -0.29; P=0.007) from baseline to endline compared to the control group. No significant group differences occurred in mean 20 m shuttle run performance and VO2 max (P>0.05) estimates.

Conclusions:We could show that intestinal parasite infections have a small but significant negative effect on the physical fitness of children, as expressed by their estimated maximal oxygen uptake. In addition, our results indicate that boys who are infected with multiple intestinal parasite species have lower physical fitness (VO2 max) levels than their non-infected peers. A significantly higher T. trichiura prevalence was noted in stunted children and those with a significantly lower Hb level, compared to children not infected with helminths of this species. A clear impact of STH infections on anthropometric indicators was also observed. A single 400 mg oral dose of albendazole was efficacious against A. lumbricoides infections but did not effectively manage T. trichiura infections, corroborating earlier research evidence. The local health and education authorities confirmed that deworming has been neglected in recent years. Biannual mass deworming is recommended in order to control the morbidity due to STH infections in two schools, annual deworming should be implemented in another school, while a test-and-treat approach appears appropriate in the other study schools. Moreover, water, sanitation and hygiene (WASH) interventions are warranted. The high spatial heterogeneity suggests that data from additional schools in different neighbourhoods will be needed to identify a more generally applicable intervention strategy.

The promotion of extra-curricular physical activity and healthy nutrition interventions should become an integral part of school health in order to improve children’s health in terms of BMI, thickness or skinfolds and cardiorespiratory fitness as indicators for the risk of chronic lifestyle conditions. While our intervention was developed by physical education specialists in consultation with local stakeholders, its effect was limited, suggesting a longer and more intensive implementation might be needed to achieve more relevant impact. Careful adaptation will be necessary before the intervention can be scaled or implemented in other settings.