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Volume 80 • Number 10




Norovirus is a pathogenic RNA virus that

is the leading cause of acute gastroenteritis

from contaminated food in the U.S. Out-

breaks occur in restaurants, schools, hotels,

home care facilities, cruise ships, and in

the wilderness tourism industry. Norovirus

outbreaks occur often during times of low

humidity such as the winter season in tem-

perate zones (Colas de la Noue et al., 2014;

Jones, Gaither, Kramer, & Gerba, 2009; Seitz

et al., 2011). These viruses are a major con-

cern for surfaces and fomites in the food pro-

duction, service, and grocery retail industries

(U.S. Department of Health and Human Ser-

vices, 2018).

The objective of this study was to test a

hypothesized norovirus transmission path-

way via reusable grocery bags (RGBs) within

a conventional grocery supermarket. A true

norovirus transmission pathway is not possi-

ble to evaluate in a public setting, so a bacte-

riophage is used as a safe surrogate to assess

the presence and concentration of the virus.

A surrogate is defined here as an organism,

particle, or substance that is used to study

the fate and transport of a pathogen in a spe-

cific environment (Sinclair et al., 2012).

The MS2 bacteriophage is a suitable surro-

gate for norovirus because it is a single-stranded

RNA virus with a similar structure and size to

most noroviruses (Beamer et al., 2014). The

MS2 bacteriophage surrogate can be used to

model the survival, morphology, and trans-

port characteristics of norovirus without the

infection risk or the necessity of mammalian

cell culture facilities (Dawson, Paish, Staffell,

Seymour, & Appleton, 2005). This experi-

ment models norovirus transmission with the

surrogate MS2 introduced into a grocery store

through an experimentally contaminated RGB.

This study builds on a previous work that

investigated the potential for contamination

in RGBs. The findings were that over 10% of

all bags obtained from shoppers contained

fecal indicator bacteria and that only 3% of

all shoppers had reported ever washing their

bags (Williams, Gerba, Maxwell, & Sinclair,

2011). Other studies have linked reusable

bags with a norovirus outbreak in the U.S.

Northwest (Repp & Keene, 2012) where

an RGB was contaminated with aerosolized

norovirus from an infected individual. This

study investigates the potential for contami-

nated RGBs to distribute viruses within a

public grocery store.

This study’s hypothesis is that norovirus

could be spread from a contaminated RGB to

various public surfaces in the grocery store

(Figure 1). The study purpose is to provide

data that can help identify critical control

Ryan Sinclair, MPH, PhD

Lindsay Fahnestock, MPH

Loma Linda University School

of Public Health

Andre Feliz, MS, MD

Environmental Safety Alliance

Jaimini Patel, MPH, REHS

Loma Linda University School

of Public Health

Christopher Perry, PhD

Loma Linda University Division of

Biochemistry, School of Medicine

Abs t r ac t

The conventional supermarket represents an

important public access to a wide variety of food that is vital for healthy

families. The supermarket is also a location where food, the public, and

pathogens can meet. The purpose of this study was to develop and test

a hypothesized norovirus transmission pathway via reusable grocery bags

(RGBs) within a conventional grocery supermarket. An RGB was inoculated

with a surrogate virus to assess potential transport of pathogens within

a grocery store. Volunteer shoppers were given an RGB sprayed with a

surrogate (bacteriophage MS2) upon entry to a grocery store. A surrogate

is defined in this study as an organism, particle, or substance that is used

to study the fate and transport of a pathogen in a specific environment

(Sinclair, Rose, Hashsham, Gerba, & Haas, 2012). The study personnel

swabbed all surfaces touched by the volunteer shopper to recover the MS2

surrogate. The data show that MS2 spread to all surfaces touched by the

shopper; the highest concentration occurred on the shopper’s hands, the

checkout stand, and the clerk’s hands. The high concentration of MS2 on

hands justify a recommendation for in-store hand hygiene as a primary

preventive measure against transmission of infectious pathogens. The high

concentrations on the checkout stand justify a secondary recommendation

for surface disinfection and public education about washing RGBs.

The Spread of a

Norovirus Surrogate

via Reusable Grocery

Bags in a Grocery