Evaluation of copromicroscopy and serology to measure the exposure to Ascaris infections across age groups and to assess the impact of 3 years of biannual mass drug administration in Jimma Town, Ethiopia

Background The scientific community has recently summarized the desired characteristics for diagnostic tools across the different phases of a soil-transmitted helminth (STH) mass drug administration (MDA) program. Although serology meets some of the desired criteria, there is a scarcity of data on baseline serological profiles in human populations, both prior to and during MDA programs. Methods In this study, we compared the copromicroscopic and the serological infection profiles in 600 school-aged children (SAC) and 600 adults at the advent of the MDA program in Jimma Town, Ethiopia. The serological profiles were examined by two ELISAs that measure IgG4 responses to the Ascaris suum haemoglobin antigen (AsHb) and a somatic extract of lung stage larvae (AsLungL3). Three years into the MDA program, we sampled another group of 600 SAC from the same schools to assess the reduction in prevalence and intensity of Ascaris infections measured by copromicroscopy and serology. Principal findings Prior to the start of MDA, copromicroscopy revealed an Ascaris prevalence of 31.0% and a mean fecal egg count of 2,919 eggs per gram (EPG) in SAC. Following three years of biannual treatment, the prevalence reduced to 13.2% (57.8% reduction) and the mean fecal egg count to 1,513 EPG (48.1% reduction). This reduction was also reflected in the serological results. The seroprevalence reduced with 40.9% and 27.4% and the mean optical density ratio reduced with 44.2% and 38.2% as measured by the AsHb or AsLungL3 ELISA respectively. We also showed that, despite a decreasing coproprevalence, seroprevalence to Ascaris increased with age. Conclusions This study is the first to provide IgG4 response profiles of an endemic population to two different A. suum antigens. The results suggest that exposure to the infectious stages of Ascaris reaches beyond SAC alone. Furthermore, it highlights the possible use of serological assays to monitor changes in STH exposure during MDA programs.
Author summary Worldwide, there has been an upscale in deworming programs to reduce the disease burden attributable to intestinal worms (giant roundworms, whipworms and hookworms). As a consequence of this, there is a focus-shift from morbidity control towards breaking transmission and ultimately disease elimination. Current standard diagnostic tools, which are based on the demonstration and quantification of worm eggs in stool (copromicroscopy), lack the diagnostic performance to make well-founded decisions when a program reaches its endgame. The scientific community has therefore defined minimal criteria that new potential diagnostic methods should meet. Diagnostic tools that are based on the detection of antibodies, which are indicative of the natural immune response of the host to worm-specific components in blood, potentially meet these criteria. We compared giant roundworm infection profiles by copromicroscopy and two antibody-based tests in both children and adults in an endemic setting. Three years into the national deworming program, another group of children from the same schools were sampled to evaluate the program progress. Our results provide a first step in the evaluation of antibodies as a diagnostic tool in the endgame of deworming programs, but they also highlight the need for further research on the interpretation of antibody-based diagnostics for STH.