skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, February 13 until 2:00 AM ET on Friday, February 14 due to maintenance. We apologize for the inconvenience.


Title: Coronavirus sampling and surveillance in bats from 1996–2019: a systematic review and meta-analysis
Abstract

The emergence of SARS-CoV-2 highlights a need for evidence-based strategies to monitor bat viruses. We performed a systematic review of coronavirus sampling (testing for RNA positivity) in bats globally. We identified 110 studies published between 2005 and 2020 that collectively reported positivity from 89,752 bat samples. We compiled 2,274 records of infection prevalence at the finest methodological, spatiotemporal and phylogenetic level of detail possible from public records into an open, static database named datacov, together with metadata on sampling and diagnostic methods. We found substantial heterogeneity in viral prevalence across studies, reflecting spatiotemporal variation in viral dynamics and methodological differences. Meta-analysis identified sample type and sampling design as the best predictors of prevalence, with virus detection maximized in rectal and faecal samples and by repeat sampling of the same site. Fewer than one in five studies collected and reported longitudinal data, and euthanasia did not improve virus detection. We show that bat sampling before the SARS-CoV-2 pandemic was concentrated in China, with research gaps in South Asia, the Americas and sub-Saharan Africa, and in subfamilies of phyllostomid bats. We propose that surveillance strategies should address these gaps to improve global health security and enable the origins of zoonotic coronaviruses to be identified.

 
more » « less
Award ID(s):
2213854 2021909
PAR ID:
10415868
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Nature Microbiology
Volume:
8
Issue:
6
ISSN:
2058-5276
Format(s):
Medium: X Size: p. 1176-1186
Size(s):
p. 1176-1186
Sponsoring Org:
National Science Foundation
More Like this
  1. Sampling reservoir hosts over time and space is critical to detect epizootics, predict spillover and design interventions. However, because sampling is logistically difficult and expensive, researchers rarely perform spatio-temporal sampling of many reservoir hosts. Bats are reservoirs of many virulent zoonotic pathogens such as filoviruses and henipaviruses, yet the highly mobile nature of these animals has limited optimal sampling of bat populations. To quantify the frequency of temporal sampling and to characterize the geographical scope of bat virus research, we here collated data on filovirus and henipavirus prevalence and seroprevalence in wild bats. We used a phylogenetically controlled meta-analysis to next assess temporal and spatial variation in bat virus detection estimates. Our analysis shows that only one in four bat virus studies report data longitudinally, that sampling efforts cluster geographically (e.g. filovirus data are available across much of Africa and Asia but are absent from Latin America and Oceania), and that sampling designs and reporting practices may affect some viral detection estimates (e.g. filovirus seroprevalence). Within the limited number of longitudinal bat virus studies, we observed high heterogeneity in viral detection estimates that in turn reflected both spatial and temporal variation. This suggests that spatio-temporal sampling designs are important to understand how zoonotic viruses are maintained and spread within and across wild bat populations, which in turn could help predict and preempt risks of zoonotic viral spillover. 
    more » « less
  2. Background: recent applications of wastewater-based epidemiology (WBE) have demonstrated its ability to track the spread and dynamics of COVID-19 at the community level. Despite the growing body of research, quantitative synthesis of SARS-CoV-2 RNA levels in wastewater generated from studies across space and time using diverse methods has not been performed. Objective: the objective of this study is to examine the correlations between SARS-CoV-2 RNA levels in wastewater and epidemiological indicators across studies, stratified by key covariates in study methodologies. In addition, we examined the association of proportions of positive detections in wastewater samples and methodological covariates. Methods: we systematically searched the Web of Science for studies published by February 16th, 2021, performed a reproducible screening, and employed mixed-effects models to estimate the levels of SARS-CoV-2 viral RNA quantities in wastewater samples and their correlations to the case prevalence, the sampling mode (grab or composite sampling), and the wastewater fraction analyzed ( i.e. , solids, solid–supernatant mixtures, or supernatants/filtrates). Results: a hundred and one studies were found; twenty studies (671 biosamples and 1751 observations) were retained following a reproducible screening. The mean positivity across all studies was 0.68 (95%-CI, [0.52; 0.85]). The mean viral RNA abundance was 5244 marker copies per mL (95%-CI, [0; 16 432]). The Pearson correlation coefficients between the viral RNA levels and case prevalence were 0.28 (95%-CI, [0.01; 0.51]) for daily new cases or 0.29 (95%-CI, [−0.15; 0.73]) for cumulative cases. The fraction analyzed accounted for 12.4% of the variability in the percentage of positive detections, followed by the case prevalence (9.3% by daily new cases and 5.9% by cumulative cases) and sampling mode (0.6%). Among observations with positive detections, the fraction analyzed accounted for 56.0% of the variability in viral RNA levels, followed by the sampling mode (6.9%) and case prevalence (0.9% by daily new cases and 0.8% by cumulative cases). While the sampling mode and fraction analyzed both significantly correlated with the SARS-CoV-2 viral RNA levels, the magnitude of the increase in positive detection associated with the fraction analyzed was larger. The mixed-effects model treating studies as random effects and case prevalence as fixed effects accounted for over 90% of the variability in SARS-CoV-2 positive detections and viral RNA levels. Interpretations: positive pooled means and confidence intervals in the Pearson correlation coefficients between the SARS-CoV-2 viral RNA levels and case prevalence indicators provide quantitative evidence that reinforces the value of wastewater-based monitoring of COVID-19. Large heterogeneities among studies in proportions of positive detections, viral RNA levels, and Pearson correlation coefficients suggest a strong demand for methods to generate data accounting for cross-study heterogeneities and more detailed metadata reporting. Large variance was explained by the fraction analyzed, suggesting sample pre-processing and fractionation as a direction that needs to be prioritized in method standardization. Mixed-effects models accounting for study level variations provide a new perspective to synthesize data from multiple studies. 
    more » « less
  3. Habitat degradation can increase zoonotic disease risks by altering infection dynamics in wildlife and increasing wildlife–human interactions. Bats are an important taxonomic group to consider these effects, because they harbour many relevant zoonotic viruses and have species‐ and context‐dependent responses to degradation that could affect zoonotic virus dynamics. Yet our understanding of the associations between habitat degradation and bat virus prevalence and seroprevalence are limited to a small number of studies, which often differ in the bats or viruses sampled, the study region, and methodology. To develop a broad understanding of the associations between bat viruses and habitat degradation, we conducted an initial phylogenetic meta‐analysis that combines published prevalence and seroprevalence (‘(sero)prevalence') with remote‐sensing habitat degradation data. Our dataset includes 588 unique records of (sero)prevalence across 16 studies, 64 bat species, and five virus families. We quantified the overall strength and direction of the relationship between habitat degradation and bat virus outcomes and tested how this relationship is moderated by the time between habitat degradation and bat sampling and by ecological traits of bat hosts while controlling for phylogenetic non‐independence among bat species. We found no effect of degradation on prevalence overall, although a weak effect may exist when forest loss occurs the year prior to bat sampling. In contrast, we detected a negative but weak association between degradation and seroprevalence overall that was strengthened when forest loss occurred the year prior to bat sampling. No bat traits that we investigated interacted with habitat degradation to impact virus outcomes, suggesting observed trends are independent of these traits. Biases in our initial dataset highlight opportunities for future work; prevalence was highly zero‐inflated, and seroprevalence was dominated byDesmodus rotundusand rabies virus. These findings and subsequent analyses will improve our understanding of how global change affects host–pathogen dynamics.

     
    more » « less
  4. null (Ed.)
    Australia’s 81 bat species play vital ecological and economic roles via suppression of insect pests and maintenance of native forests through pollination and seed dispersal. Bats also host a wide diversity of coronaviruses globally, including several viral species that are closely related to SARS-CoV-2 and other emergent human respiratory coronaviruses. Although there are hundreds of studies of bat coronaviruses globally, there are only three studies of bat coronaviruses in Australian bat species, and no systematic studies of drivers of shedding. These limited studies have identified two betacoronaviruses and seven alphacoronaviruses, but less than half of Australian species are included in these studies and further research is therefore needed. There is no current evidence of spillover of coronaviruses from bats to humans in Australia, either directly or indirectly via intermediate hosts. The limited available data are inadequate to determine whether this lack of evidence indicates that spillover does not occur or occurs but is undetected. Conversely, multiple international agencies have flagged the potential transmission of human coronaviruses (including SARS CoV-2) from humans to bats, and the consequent threat to bat conservation and human health. Australia has a long history of bat research across a broad range of ecological and associated disciplines, as well as expertise in viral spillover from bats. This strong foundation is an ideal platform for developing integrative approaches to understanding bat health and sustainable protection of human health. 
    more » « less
  5. Tully, Damien (Ed.)
    Virus host shifts are generally associated with novel adaptations to exploit the cells of the new host species optimally. Surprisingly, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has apparently required little to no significant adaptation to humans since the start of the Coronavirus Disease 2019 (COVID-19) pandemic and to October 2020. Here we assess the types of natural selection taking place in Sarbecoviruses in horseshoe bats versus the early SARS-CoV-2 evolution in humans. While there is moderate evidence of diversifying positive selection in SARS-CoV-2 in humans, it is limited to the early phase of the pandemic, and purifying selection is much weaker in SARS-CoV-2 than in related bat Sarbecoviruses . In contrast, our analysis detects evidence for significant positive episodic diversifying selection acting at the base of the bat virus lineage SARS-CoV-2 emerged from, accompanied by an adaptive depletion in CpG composition presumed to be linked to the action of antiviral mechanisms in these ancestral bat hosts. The closest bat virus to SARS-CoV-2, RmYN02 (sharing an ancestor about 1976), is a recombinant with a structure that includes differential CpG content in Spike; clear evidence of coinfection and evolution in bats without involvement of other species. While an undiscovered “facilitating” intermediate species cannot be discounted, collectively, our results support the progenitor of SARS-CoV-2 being capable of efficient human–human transmission as a consequence of its adaptive evolutionary history in bats, not humans, which created a relatively generalist virus. 
    more » « less