Wastewater testing during the South African 2022-2023 measles outbreak demonstrates the potential of environmental surveillance to support measles elimination

Abstract

AbstractBackgroundSensitive clinical surveillance and high vaccination coverage are required to meet the WHO 2030 measles elimination target. Whilst wastewater and environmental surveillance (WES) has proven usefulness in polio surveillance, it has not been applied to measles control. We describe the development of digital RT-PCR (RT-dPCR) for detection and quantification of measles virus (MeV) in wastewater, and application to retained concentrated samples obtained from 28 national sentinel SARS-CoV-2 wastewater surveillance sites and 19 localised collection points in a single province before, during and after a measles outbreak of over 2,000 laboratory-confirmed cases.MethodsWe validated a RT-dPCR assay incorporating WHO-recommended primers for detection and differentiation of wild-type and vaccine genotypes. We applied this to retained wastewater samples concentrated by ultrafiltration and stored at −20°C. We compared wastewater findings by district and epidemiological weeks with laboratory-confirmed measles case data obtained from national fever-rash surveillance for districts with adequate surveillance indicators (>2/100,000 non-measles cases)FindingsAmongst 2,149 wastewater concentrates obtained between 16 February 2021 and 08 March 2024, we identified 43 (2%) samples containing MeV RNA in concentrations ranging from 2,04-6,11 genome copies/mL. MeV genotype A (vaccine strain) was co-detected in wastewater in 6 instances along with non-A (wild-type) genotypes. Comparison of wastewater and clinical fever-rash surveillance data by epidemiological week and district identified 27 district-time instances where at least one positive wastewater sample was identified, of which 14 (52%) districts reported at least one laboratory-confirmed clinical case in that same epidemiological week. Amongst districts with positive wastewater samples, wastewater surveillance detected MeV in 13/27 (48%) time-district pairs when clinical surveillance failed to detect cases. Amongst district-time instances where at least one laboratory-confirmed measles case was detected (N=127), MeV was detected in at least one wastewater sample collected in that same epidemiological week in 14 (11%) districtsInterpretationWastewater surveillance may be a useful complementary surveillance tool for identification of districts with ongoing measles circulation. MeV detection rates may be improved by real-time testing to limit RNA degradation and improved concentration and nucleic acid extraction processes. Ongoing wastewater surveillance for MeV should be conducted in order to understand the role of WES in measles control and elimination.FundingThis work was funded by BMGF (INV-049271)