Virus Inactivation on Hard Surfaces or in Suspension by Chemical Disinfectants: Systematic Review and Meta-Analysis of Norovirus Surrogates

Abstract

Norovirus (NoV) infections are the leading cause of foodborne illness in the United States. Effective disinfection is important for controlling outbreaks caused by this highly infectious virus but can be difficult to achieve because NoV is very resistant to many common disinfection protocols. The inability of human NoV to replicate in tissue culture complicates NoV research, generally necessitating genome copy quantification, the use of surrogate viruses, or the use of other substitutes such as virus-like particles. To date, comprehensive comparisons among NoV surrogates and between surrogates and human NoV are missing, and it is not clear how best to extrapolate information from surrogate data. We conducted a systematic review and meta-analysis of comparisons of NoV surrogates with regard to their susceptibility to disinfection on hard surfaces or in suspension. Restricting our analysis to those studies in which two or more virus surrogates were compared allowed us to improve the signal-to-noise ratio in our analysis, similar to the epidemiological concept of matching. Using meta-analysis methods, our results indicate that hepatitis A virus, murine norovirus 1, and phage MS2 are significantly more resistant to disinfection than is feline calicivirus, but average differences in viral titer reduction appeared to be modest, 1.5 log PFU or less in all cases. None of the studies that compared surrogates and human NoV met our inclusion criteria, precluding a direct comparison between human NoV and NoV surrogates in this study. For all surrogates with sufficient data available to permit subgroup analyses, we detected strong evidence that the type of disinfectant impacted the relative susceptibility of the surrogates. Therefore, extrapolation of results between surrogates or from surrogates to human NoV must consider the type of disinfectant studied.