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International Journal of Food Microbiology
journal homepage: www.elsevier.com/locate/ijfoodmicro
UV-C inactivation of foodborne bacterial and viral pathogens and surrogates
on fresh and frozen berries
Sophie Butot
a
, Frédérique Cantergiani
a
, Mireille Moser
a
, Julie Jean
b
, Anthony Lima
a
,
Lise Michot
a
, Thierry Putallaz
a
, Thomas Stroheker
a
, Sophie Zuber
a,
⁎
a
Nestlé Research Center, Institute of Food Safety and Analytical Science, CH 1000, Lausanne 26, Switzerland
b
Institute of Nutrition and Functional Foods, Université Laval, Quebec, Quebec G1V 0A6, Canada
ARTICLE INFO
Keywords:
Inactivation
Ultraviolet
Food
Berries
Bacteria
Virus
ABSTRACT
Outbreaks of foodborne illness associated with berries often involve contamination with hepatitis A virus (HAV)
and norovirus but also bacteria such as Escherichia coli O157:H7 and parasites such as Cyclospora caytanensis. We
evaluated the applicability of UV-C to the inactivation of pathogens on strawberries, raspberries and blueberries.
Our three-step approach consisted of assessing the chemical safety of UV-C-irradiated berries, evaluating the
sensory quality after UV-C treatment and finally studying the inactivation of the target microorganisms.
Treatments lasting up to 9 min (4000 mJ cm
-2
) did not produce detectable levels of furan (< 5 μg/kg), a known
photolysis product of fructose with genotoxic activity and thus were assessed to be toxicologically safe. No effect
on taste or appearance was observed, unless treatment was excessively long. 20 s of treatment (an average
fluence of ~ 212 mJ cm
-2
) reduced active HAV titer by > 1 log
10
unit in 95% of cases except on frozen rasp-
berries, while 120 s were required to inactivate murine norovirus to this extent on fresh blueberries. The mean
inactivation of HAV and MNV was greater on blueberries (2–3 log
10
) than on strawberries and raspberries (< 2
log
10
). MNV was more sensitive on fresh than on frozen berries, unlike HAV. Inactivation of Salmonella, E. coli
O157:H7 and Listeria monocytogenes was poor on all three berries, no treatment reducing viable counts by > 1
log
10
unit. In most matrices, prolonging the treatment did not improve the result to any significant degree. The
effect was near its plateau after 20 s of treatment. These results provide insight into the effectiveness of UV-C
irradiation for inactivating bacterial and viral pathogens and surrogates on fresh and frozen berries having
different surface types, under different physical conditions and at different levels of contamination. Overall they
show that UV-C as single processing step is unsuitable to inactivate significant numbers of foodborne pathogens
on berries.
1. Introduction
In its quest to continue to provide non-perishable foods that are of
high quality in terms of enjoyment, nutrition and safety in post-in-
dustrial society, the food industry faces a variety of emergent chal-
lenges. According to estimates, 31 foodborne agents caused 600 million
illnesses worldwide in 2010 (World Health Organization, 2015). Fruits
and vegetables are recognized as a major source of disease outbreaks,
and the potential sources of contamination in the supply chain at both
the pre-harvest (in the field) and post-harvest stages are various. As
reviewed previously (Berger et al., 2010), the use of contaminated
water for irrigation or rinsing, application of inadequately composted
manures or raw sewage, contact with insects, storage and processing
are all possible sources of contamination. Freezing remains a wide-
spread practice for increasing the convenience and shelf life of highly
perishable products. Frozen fruits are widely distributed and used as
ingredients in many foods such as cakes, yogurts and smoothies.
The most common pathogens transmitted by fruits and vegetables
are human noroviruses (40%), followed by Salmonella (18%),
Escherichia coli O157:H7 (8%), Clostridium (6%), the hepatitis A virus
(4%), Shigella (4%), Bacillus (3%) and Staphylococcus (3%) (Doyle and
Erickson, 2008). Numerous outbreaks of hepatitis A virus (HAV) and
norovirus have been reported in association with consumption of fresh
or frozen fruits such as blueberries (Calder et al., 2003), strawberries
(Bernard et al., 2014; Montaño-Remacha et al., 2014; Niu et al., 1992;
Nordic outbreak investigation team, 2013), raspberries (Gaulin et al.,
1999; Le Guyader et al., 2004; Pönkä et al., 1999) and pomegranate
arils (Collier et al., 2014; Swinkels et al., 2014). Foodborne parasites
have also been associated with outbreaks linked to berries, for example
cyclosporiasis associated with raspberries (Herwaldt, 2000). The EFSA
https://doi.org/10.1016/j.ijfoodmicro.2018.03.016
Received 13 October 2017; Received in revised form 13 February 2018; Accepted 20 March 2018
⁎
Corresponding author.
E-mail address: sophie.zuber@rdls.nestle.com (S. Zuber).
International Journal of Food Microbiology 275 (2018) 8–16
Available online 26 March 2018
0168-1605/ © 2018 Published by Elsevier B.V.
T