Polio and Measles Down the Drain: Environmental Enterovirus Surveillance in the Netherlands, 2005 to 2015

Abstract

Polioviruses (PVs) are members of the genus Enterovirus. In the Netherlands, the exclusion of PV circulation is based on clinical enterovirus (EV) surveillance (CEVS) of EV-positive cases and routine environmental EV surveillance (EEVS) conducted on sewage samples collected in the region of the Netherlands where vaccination coverage is low due to religious reasons. We compared the EEVS data to those of the CEVS to gain insight into the relevance of EEVS for poliovirus and nonpolio enterovirus surveillance. Following the polio outbreak in Syria, EEVS was performed at the primary refugee center in Ter Apel in the Netherlands, and data were compared to those of CEVS and EEVS. Furthermore, we assessed the feasibility of poliovirus detection by EEVS using measles virus detection in sewage during a measles outbreak as a proxy. Two Sabin-like PVs were found in routine EEVS, 11 Sabin-like PVs were detected in the CEVS, and one Sabin-like PV was found in the Ter Apel sewage. We observed significant differences between the three programs regarding which EVs were found. In 6 sewage samples collected during the measles outbreak in 2013, measles virus RNA was detected in regions where measles cases were identified. In conclusion, we detected PVs, nonpolio EVs, and measles virus in sewage and showed that environmental surveillance is useful for poliovirus detection in the Netherlands, where live oral poliovirus vaccine is not used and communities with lower vaccination coverage exist. EEVS led to the detection of EV types not seen in the CEVS, showing that EEVS is complementary to CEVS. IMPORTANCE We show that environmental enterovirus surveillance complements clinical enterovirus surveillance for poliovirus detection, or exclusion, and for nonpolio enterovirus surveillance. Even in the presence of adequate surveillance, only a very limited number of Sabin-like poliovirus strains were detected in a 10-year period, and no signs of transmission of oral polio vaccine (OPV) strains were found in a country using exclusively inactivated polio vaccine (IPV). Measles viruses can be detected during an outbreak in sewage samples collected and concentrated following procedures used for environmental enterovirus surveillance.

Detection of Enterovirus D68 in wastewater samples from the United Kingdom during outbreaks reported globally between 2015 and 2018

“…Nevertheless, EV-D68 was frequently detected in wastewater samples during reported outbreaks despite the fact that the virus is rarely found in stools from clinical cases (Barnadas et al 2017, Van Leer-Buter et al 2016). Although the presence of EV-D68 in sewage has been reported before (Benschop et al 2017, Brinkman et al 2017, Weil et al 2017), our finding was unexpected and suggests that EV-D68 might replicate in the gut more commonly than it is thought, perhaps during the initial stages of infection before respiratory symptoms develop and samples are collected for analysis. Although unlikely, the possibility that EV-D68 present in human respiratory fluids could reach the sewage system through washing, showering, etc.…”

Detection by Direct Next Generation Sequencing Analysis of Emerging Enterovirus D68 and C109 Strains in an Environmental Sample From Scotland

“…The most prevalent strains belonged to species B serotypes but EV strains from species A (CV-A4, CV-A6, and CV-A16), C (CV-A1, CV-A22, and EV-C109), and D (EV-D68) serotypes were also found. Previous studies have shown a high frequency of EV-B strains in Europe and the United States with the occasional expansion of EV-A and EV-D serotypes such as CV-A6, CV-A16, EV-A71, or EV-D68 ( Benschop et al, 2017 ; Brinkman et al, 2017 ). However, a high number of EV-C strains in sewage samples have been reported before in Scotland using direct PCR with EV species-specific primers ( Harvala et al, 2014 ).…”

Environmental Surveillance Reveals Complex Enterovirus Circulation Patterns in Human Populations

“…EV-D strains (all from serotype EV-D68) were only found in sewage samples from the United Kingdom. Studies using a variety of cell lines or direct molecular typing have shown the prevalence of EV-B strains in sewage in Europe and the United States (typically >75% of all EVs), with the occasional upsurge of EV-A and EV-D serotypes in recent years [ 15 , 21 ]. Interestingly, a recent study in Scotland identified a high quantity of EV-C strains in sewage samples (95 amplicons from 353 cloned EV sequences, 26.9%) [ 14 ].…”