Epidemiology and burden of soil-transmitted helminth infections among school-aged Bulang children in Yunnan province, People's Republic of China

Background: The three most common soil-transmitted helminths are Ascaris lumbricoides (roundworm), Trichuris trichiura (whipworm), and Ancylostoma duodenale and Necator americanus (hookworms). Collectively, they infect around 1 billion people and put approximately 5 billion people at risk of infection worldwide. Strongyloides stercoralis is a less common soil-transmitted helminth than the species mentioned above, but still significant from a public health perspective. The global prevalence of S. stercoralis is estimated to be 30-100 million. Populations most affected by these parasitic worms are often impoverished, living on less than US$ 2 per day, and have poor sanitation facilities and hygiene habits. Despite the low prevalence levels of soil-transmitted helminth infections observed on a national level in the People’s Republic of China (P.R. China), hotspots of these infections, particularly within ethnic minority groups residing in rural areas, still exist.
Single-species infections with the common soil-transmitted helminths can cause symptoms ranging from abdominal pain to anaemia, and impaired development of cognitive abilities. For S. stercoralis infections, symptoms such as severe abdominal pain and blood in the stool have been reported. Due to the chronic and subtle nature of most morbidities commonly associated with soil-transmitted helminthiasis, it is difficult to assess the true burden due to these infections.
Objectives: The goal guiding this Ph.D. project was to deepen the understanding of the epidemiology and burden of soil-transmitted helminthiasis among school-aged children from the Bulang ethnic minority group in P.R. China. The following objectives were pursued: (i) to evaluate the feasibility of deploying different tools for the assessment of physical fitness in soil-transmitted helminth-endemic settings; (ii) to monitor changes in physical fitness, strength and anthropometric measurements over a six-month period among treated children and their untreated peers; (iii) to predict and visualize the change in physical fitness of school-aged children due to soil-transmitted helminth infections over a 1-month period across P.R. China; (iv) to assess the efficacy of triple-dose albendazole and study soil-transmitted helminth re-infection patterns after deworming; and (v) to estimate the odds of re-infection with soil-transmitted helminths for different natural nutritional statuses and types of nutritional supplementation.
Methods: For the field studies, parasitological examination of stool samples was performed. The Kato-Katz technique was used to identify the eggs of A. lumbricoides, hookworm, T. trichiura and other helminths, while the Baermann technique was used to identify the larvae of S. stercoralis. In addition, each stool sample was visually inspected for Taenia spp. proglottids. Physical fitness was estimated with the 20-m shuttle run test and physical strength was assessed with the grip strength and standing broad jump tests. Anthropometric measurements, including body height and weight and sum of skinfolds, and haemoglobin level were also recorded. Physical fitness and strength scores, anthropometric measurements, and haemoglobin level were expressed as means, and compared among children of distinct soil-transmitted helminth infection status and intensity. For the prediction and visualization exercise, the change in physical fitness over 1 month across P.R. China was predicted over a smooth surface of soil-transmitted helminth risk. Maps, with lower and upper boundaries of the predicted values as well as population-adjusted estimates, were further created. Finally, for the systematic review, the odds of re-infection with soil-transmitted helminths for different natural nutritional statuses and types of nutritional supplementation were estimated and qualitative content analysis was conducted for all studies included in the review.
Results: In a cross-sectional survey, the maximum aerobic capacity in 1 min of exhaustive exercise (VO2 max estimate) of T. trichiura-infected children was 1.9 ml kg-1 min-1 lower than that of their non-infected counterparts (P=0.01). Until exhaustion, T. trichiura-infected children had completed six 20-m laps less (P<0.01). No significant association between anthropometric indicators and infection with any soil-transmitted helminth species could be established.
In a randomised controlled trial, which investigated the effects of triple-dose albendazole on physical fitness of school-aged children, baseline prevalences of T. trichiura, A. lumbricoides, hookworm, and S. stercoralis were 94.5%, 93.3%, 61.3%, and 3.1% respectively, with more than half harboring triple-species infections. During the course of the trial, rapid re-infection with A. lumbricoides was observed and low cure rate was achieved with T. trichiura infections. Children receiving triple-dose albendazole scored slightly higher values in physical fitness and strength scores, anthropometric measurements, and haemoglobin level than placebo recipients, but the difference lacked statistical significance. The increase in VO2 max estimate from baseline was 1.6 ml kg-1 min-1 (P=0.02) less and the increase in the number of 20-m laps completed from baseline was five 20-m laps (P=0.04) less for T. trichiura-infected children compared to their non-infected peers. In addition, children with low infection intensity of T. trichiura and hookworm had consistently more increase in the VO2 max estimate from baseline than their peers with high infection intensity of all soil-transmitted helminths (range: 1.9-2.1 ml kg-1 min-1; all P <0.05).
In the systematic review, multi-micronutrients seemed to have the clearest effect with regards to lowering re-infection rates and intensity of soil-transmitted helminths, whereas consumption of zinc or vitamin A alone might have a negative impact on these two outcomes measures. With regards to the natural nutrition status of the host, the general trend observed was that individuals with poor nutrition status suffered higher re-infection rates and intensities when compared to their well-nourished peers. Overall, only fifteen studies met our inclusion criteria and majority of them were of low quality.
Conclusions/significance: The negative associations observed between T. trichiura infections and physical fitness among school-aged Bulang children in Yunnan suggests that the current burden estimate of soil-transmitted helminth infections, in particular T. trichiura infections, might be underestimated and there are still subtle and hidden morbidities to be quantified. A paradigm shift is needed to further understand the burden of soil-transmitted helminth infections as the presence of co-infections and co-morbidities add layers of complexity to the task. Finally, the epidemiological findings on soil-transmitted helminthiasis from this thesis highlight that a national soil-transmitted helminth control programme is overdue and urgently needed as P.R. China further develops into a global powerhouse. With many of their rural communities starting to have their hands on the first rung of the development ladder, P.R. China seems to be in a good position to set a leading example on how to control and eliminate soil-transmitted helminthiasis, and possibly other neglected tropical diseases, for developing countries around the world.