MC Leod

Received: 21 June 2017 | Revised: 20 September 2017 | Accepted: 19 October 2017
DOI: 10.1111/jfs.12421
ORIGINAL ARTICLE
Chicken fillets subjected to UV-C and pulsed UV light:

Reduction of pathogenic and spoilage bacteria, and changes
in sensory quality
Anette McLeod | Kristian Hovde Liland | John-Erik Haugen | Oddvin Sørheim |

Kristine S. Myhrer | Askild L. Holck
Nofima, Norwegian Institute of Food,

Fisheries and Aquaculture Research, Ås,
Abstract
Norway We have compared the efficacy of continuous ultraviolet (UV-C) (254 nm) and pulsed UV light in
reducing the viability of Salmonella Enteritidis, Listeria monocytogenes, Staphylococcus aureus, enter-
Correspondence
ohemorrhagic Escherichia coli, Pseudomonas spp., Brochothrix thermospacta, Carnobacterium
Askild L. Holck, Nofima, Norwegian
Institute of Food, Fisheries and Aquaculture divergens, and extended-spectrum b-lactamase producing E. coli inoculated on chicken fillet sur-
Research, P.O. Box 210, N-1431 Ås, face. Fluences from 0.05 to 3.0 J/cm2 (10 mW/cm2, from 5 to 300 s) used for UV-C light resulted
Norway. in average reductions from 1.1 to 2.8 log cfu/cm2. For pulsed UV light, fluences from 1.25 to 18.0
Email: [email protected]
J/cm2 gave average reductions from 0.9 to 3.0 log cfu/cm2. A small change in the odor character-
Funding information ized as sunburnt and increased concentration of volatile compounds associated with burnt odor
The Research Council of Norway, Grant/ posed restrictions on the upper limit of UV treatment, however no sensory changes were observed
Award Number: 221663; Foundation for
after cooking the meat. Treatments under modified atmosphere conditions using a UV permeable
Research Levy on Agricultural Products,
Grant/Award Number: 262306 top film gave similar or slightly lower bacterial reductions.
Practical applications
The copyright line for this article was
changed on 30 July 2018 after original Ultraviolet (UV) light may be used for decontaminating the surface of food products and reduce
online publication. viability of pathogenic and spoilage bacteria. Exposure of raw chicken fillet surface to various
doses of continuous UV-C or pulsed UV light proposed in the present work represent alternatives
for microbiological improvement of this product. Chicken fillets can be treated in intact packages
covered with UV permeable top film, thus avoiding recontamination of the meat. UV-C light treat-
ment is a low cost strategy with low maintenance, whereas pulsed UV light involves more
elaborate equipment, but treatment times are short and less space is required. Both methods can
be helpful for producers to manage the safety and quality of chicken fillets.
1 | INTRODUCTION microorganisms on their skin, feathers, and in their digestive tract, con-
tamination of the carcasses during slaughtering procedures cannot be
The desired long shelf life in today’s food industry has led to increasing completely avoided when live animals are converted to meat for
demands in the development of methods for improving microbial safety consumption.
and quality. According to the Food and Agriculture Organization of the Food contamination is a major global burden because of foodborne
United Nations (FAO), the average annual consumption of chicken illnesses that can result from it. Poultry may be the vector of Salmonella
meat pro capita worldwide increased from 10.2 kg in 1999 to 13.8 kg spp., Campylobacter spp., Staphylococcus aureus, Listeria monocytogenes,
in 2015 (FAO, 2015). The global meat consumption is projected to rise Shiga toxin-producing Escherichia coli, and other pathogens (Capita,
more than 4% per person over the next 10 years, and for poultry it Alonso-Calleja, Garcia-Fernandez, & Moreno, 2002; Hafez, 1999; Zhao
is predicted to rise more than 10% (Organisation for Economic et al., 2001). The first two mentioned are the most common causes of
Co-operation and Development/Food and Agriculture Organization of human foodborne bacterial diseases linked to poultry (European Food
the United Nations, 2016). As live poultry animals contain Safety Authority [EFSA], 2015; Hafez, 2005). According to the
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is
properly cited.
© 2017 The Authors. Journal of Food Safety published by Wiley Periodicals, Inc.
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https://doi.org/10.1111/jfs.12421
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2 of 15 | MCLEOD ET AL.
Community Summary Reports of the EFSA and the European Centre reaction between adjacent pyrimidine bases to form dimer lesions,
for Disease Prevention and Control, 2008, campylobacteriosis and sal- which in turn inhibit replication and transcription in cells (Harm, 1980;
monellosis accounted for 214,779 and 82,694, respectively, confirmed Weber, 2005).
human cases in the EU (EFSA, 2015). The number of confirmed listerio- As a means for controlling surface microorganisms on food prod-
sis cases in humans was 1,763, where a high fatality rate of 15.6% was ucts, regulations in conjugation with using conventional continuous
reported among the cases. Antibiotic-resistant bacteria, such as the UV-C light (henceforth referred to as UV-C light) in the United States
extended-spectrum beta-lactamase (ESBL)-producing E. coli, have are given by the U.S. Food and Drug Administration (FDA) (FDA,
become a growing public health threat (Briongos-Figuero et al., 2012; 2010). UV-C light can be employed in Europe, however, in Germany
Lu et al., 2012; Picozzi et al., 2013; Pitout, 2010). The ESBL-producing the use is limited to water, fruit and vegetable products, and stored
strains are feared as they produce the enzyme beta-lactamase that has hard cheeses (Anonymous, 2000). Decontamination of raw boneless,
the ability to break down commonly used antibiotics like penicillins and skinless chicken, or broiler breast fillets by the use of UV-C light has
cephalosporins, and render them ineffective for treatment. In 2014, the been reported to reduce bacterial counts of various pathogens by 0.6
World Health Organization (WHO) warned that the antibiotic resist- to 1.7 log depending on the conditions used (Chun, Kim, Lee, Yu, &
ance crisis is becoming dire, with diseases that have been curable Song, 2010; Haughton et al., 2011b; Isohanni & Lyhs, 2009; Sommers,
for decades becoming increasingly difficult to treat (Michael, Dominey- Scullen, & Sheen, 2016). High intensity pulsed UV light has been
Howes, & Labbate, 2014; WHO, 2014). The presence of ESBL genes approved by the FDA up to 12 J/cm2 (FDA, 2010). The UV energy
has been clearly documented in Enterobacteriaceae isolated from food- spectrum of pulsed UV light consists of a continual broadband spec-
production animals, and especially from chickens (Machado, Coque, trum from deep UV to infrared light, especially rich in UV range below
Canton, Sousa, & Peixe, 2008; Overdevest et al., 2011; Smet et al., 400 nm, which is germicidal. In addition to creating dimer lesions,
2008). Occurrence of cephalosporin-resistant E. coli on poultry in pulsed UV light has been proposed to cause cell damage and cell death
Norway ranged from 8 to 43% (Mo et al., 2014). by inducing damage of the cell membrane and to cause rupture of
Food rendered unfit for human consumption because of product the bacteria by thermal stress (Krishnamurthy, Tewari, Irudayaraj, &
spoilage results in significant economic losses when products must be Demirci, 2010; Takeshita et al., 2003; Wekhof, 2000). The use of this
removed from the market. The accumulation of metabolic by-products technology for food decontamination has previously been reviewed
or the action of extracellular enzymes produced by spoilage bacteria (Demirci & Panico, 2008; Gomez-Lopez, Ragaert, Debevere, &
multiplying on these foods, leads to deterioration like discoloration, Devlieghere, 2007). Pathogen reduction on boneless skinless chicken
texture change, and formation of off-flavors, off-odors, and slime. The breast has been reported to vary from 1.2 to 2.4 log depending on the
meat acquires an offensive odor when the bacterial flora reaches about conditions used (Keklik, Demirci, & Puri, 2010; Paskeviciute, Buchovec,
107 cfu/cm2 of the surface, and when reaching 108 cfu/cm2, the sur-
& Luksiene, 2011). Several investigations have demonstrated the effec-
face becomes slimy (Borch, Kant-Muermans, & Blixt, 1996; Holck,
tiveness of UV light on microbial reduction in vitro, and a wide range of
Pettersen, Moen, & Sorheim, 2014; Molin, 2000). The natural micro-
bacterial species were reduced by 5–7 log when treated on petri dishes
flora on chicken fillets has been identified (Holck et al., 2014), and com-
under different conditions (Farrell, Garvey, Cormican, Laffey, & Rowan,
mon spoilage microorganisms when stored aerobically at 48C are
2010; Gomez-Lopez, Devlieghere, Bonduelle, & Debevere, 2005;
Pseudomonas spp., Brochothrix spp., and Enterobacteriaceae. A widely
Paskeviciute et al., 2011; Rowan et al., 1999).
used strategy for increasing shelf life of poultry meat is modified
The objective of our investigation was to study and compare the
atmosphere packaging (MAP) (Holck et al., 2014; van Velzen &
efficacy of UV-C and pulsed UV light against pathogens and bacteria
Linnemann, 2008). Storage with high CO2 (70% CO2, 30% N2) can lead
often found as natural contaminants on fresh chicken meat, of which
to lactic acid bacteria like carnobacteria dominating the flora (Holck
several of the species have not previously been investigated for UV
et al., 2014; Vihavainen et al., 2007). Although some strains of carno-
light treatment on food. To our knowledge, studies on UV light expo-
bacteria show little influence on the sensory properties of a product,
sure of intact packages of MAP-chicken fillet for bacterial reduction
others can spoil the product (Laursen et al., 2005; Leisner, Laursen,
have not been reported, thus we aimed at undertaking this issue using
Prevost, Drider, & Dalgaard, 2007).
a UV permeable top film. We also aimed at determining whether the
Various physical and chemical methods to reduce microbes on
UV light treatments had adverse effects on the sensory quality of
poultry products have been studied, such as water spraying, air chilling,
chicken fillets.
ultrasound, irradiation, trisodium phosphate, and lactic acid (Capita
et al., 2002; Loretz, Stephan, & Zweifel, 2010). Potential disadvantages
2 | MATERIALS AND METHODS
using these methods are sensory changes, deterioration of product
appearance and quality, and safety concerns. In recent years, there has
2.1 | Bacterial strains, media, and growth conditions
been a growing interest in using ultraviolet (UV) light for decontamina-
tion of poultry. UV light is widely known for its germicidal effect by The bacterial strains used in this work are listed in Table 1. The strains
damaging nucleic acids (Kowalkski, 2009). The high energy associated were maintained at 2808C in their respective media supplemented
with short-wavelength UV energy (UV-C), primarily at 254 nm, is with 20% glycerol (vol/vol). Rifampicin resistant (RifR) derivatives were
absorbed by cellular RNA and DNA. This energy absorption initiates a prepared for all isolates by growing strains in liquid media containing
MCLEOD ET AL. | 3 of 15
TA BL E 1 Strains used in this study The different bacterial strains of each species were cultured separately.
Carnobacterium divergens was grown in cystein-deMan Rogosa Sharpe
Bacterial species Strain namea Reference/source/strain/other broth (cMRS, Oxoid) with 200 mg/ml rifampicin (Sigma-Aldrich; 48 hr
incubation, 308C), ESBL-producing E. coli in Brain Heart Infusion broth
Pseudomonas spp. MF6041 Chicken fillet
MF6042 Chicken fillet (BHI; Oxoid) with 50 mg/ml ampicillin (Sigma-Aldrich; 16 hr incubation,
MF6043 Chicken fillet 378C), and tryptic soy broth (TSB, Oxoid) with 200 mg/ml rifampicin was
MF6044 Chicken fillet
used for Pseudomonas spp. (16 hr incubation, 308C), Brochothrix thermo-
B. thermospacta MF6045 Chicken spacta (48 hr incubation, 308C), Salmonella Enteritidis, L. monocytogenes,
MF6047 Chicken S. aureus, and EHEC (16 hr incubation, 378C). Before decontamination
MF6049 ATCC11509b
experiments, bacterial cultures of each of the different strains of the
C. divergens MF3036 DSM20623c same species were mixed in equal amounts, for example, bacterial cul-
MF6031 Chicken fillet tures of each of the four strains of L. monocytogenes were mixed 1:1:1:1.
MF6032 Chicken fillet
MF6034 Chicken fillet An exception was E. coli, for which the ESBL-producing E. coli strains
MF6038 Chicken fillet and the EHEC strains were separated from each other.
ESBL-producing E. coli MF5658 Chickend

MF5660 Chickend 2.2 | UV illumination experiments of chicken and agar
MF5664 Chickend
surface inoculated with bacterial cells
MF5670 Broilerd
MF5674 Broilerd
Fresh skinless chicken breast fillets were purchased from local Norwe-
S. Enteritidis MF3817 1049-1-99 d gian supermarkets. The meat was cut into pieces of 10 cm2, and one
MF3818 Poultry, 61–358-1e side of the chicken was inoculated by spreading 15 mL suspension of a
MF3824 ATCC13076b
multi strain mix of one species (described above) to obtain bacterial lev-
L. monocytogenes MF3508 2230/92 (Nesbakken, 1995) els of 105–107 cfu/cm2. The inoculated chicken samples were left at
MF3509 167 (Blom et al., 1997) room temperature to dry for 1 hr prior to UV light treatment. To assess
MF3510 187 (Blom et al., 1997)
MF3571 EGD-e (Glaser et al., 2001)
the indigenous background flora of the chicken, uninoculated samples
were also analyzed. For in vitro illumination experiments, serial 10-fold
S. aureus MF2123 ATCC25923b
dilutions of each multi strain mix were made and plated onto the
MF2124 ATCC12600b
MF2125 ATCC6538b respective agar media (described below). In the UV-C light experiments,
samples were treated in a custom made aluminum chamber (1.0 3 0.5
Enterohemorrhagic MF3572 O103, fermented sausage, linked
E. coli (EHEC) to outbreak in Norway 2006
3 0.6) m3 equipped with two UV-C lamps (UV-C Kompaktleuchte,
(Schimmer et al., 2008)f €
2x95 W, BARO GmbH, Leichlingen, Germany) in the ceiling. The UV-C
MF3574 ATCC43895b, O157:H7 light was emitted essentially at 253.7 nm, measured using a UVX Radi-
MF3576 O111:H-, semi-dry fermented
sausage, outbreak Australia ometer (Ultra-Violet Products, Ltd., Cambridge, UK) equipped with a
1995 (Paton et al., 1996)g UV-C sensor (model UVX-25, Ultra-Violet Products). Both sample dis-
MF5554 O145 (McLeod et al., 2016)
tance (6 cm) from the lamps and duration of the exposures were cho-
a
Antibiotic resistant strains. All strains were grown in their respective sen with aim to be relevant for industrial production lines. Exposures
medium with 200 mg/ml rifampicin, except ESBL-producing E. coli grown were thus at 10 mW/cm2, which is close to a maximum when using
in medium with 50 mg/ml ampicillin.
b commercial lamps, for 5, 10, 30, 60, or 300 s, giving fluences of 0.05,
ATCC, American Type Culture Collection, Manassas, VA, USA.
c
DSM, Deutsche Sammlung von Microorganismen und Zellkulturen, 0.1, 0.3, 0.6, 3.0 J/cm2, respectively. For the pulsed UV light experi-
Braunschweig, Germany. ments, a semiautomated intense pulsed UV system instrument
d
Kindly received from the Norwegian Veterinary Institute, Oslo, Norway.
e XeMaticA-SA1L (SteriBeam Systems GmbH, Kehl-Kork am Rhein, Ger-
Kindly received from the Technical University of Denmark, the National
Veterinary Institute, Denmark. many) was used. Samples were placed in the instrument chamber at a
f
Kindly received from the Norwegian School of Veterinary Science, Oslo, 6.5 cm distance from the xenon lamp (19 cm), which was water cooled,
Norway.
g had an aluminum reflector (10 cm 3 20 cm), and the spectral distribu-
Kindly received from Statens Serum Institut, Copenhagen, Denmark.
tion was 200–1,100 nm, with up to 45% of the energy being in the
UV-region (maximal emission at 260 nm). The fluences were set
according to the manufacturers specifications, and were adjusted to
200 mg/ml rifampicin as described by Heir et al. (2010), except for the 1.25 J/cm2 (low) or 3.6 J/cm2 (high). The lowest level of exposure
ESBL-producing E. coli strains already resistant to several types of anti- would result in limited bacterial reductions, and fluences up to and
biotics. Growth experiments using a Bioscreen C instrument (Labsys- above the limit value of 12 J/cm2, which is the maximum permitted
tems) where the Optical Density (OD) at 600 nm was monitored, dose by FDA (FDA, 2010), were tested. Samples were exposed either
showed no significant difference in growth between the original strains once to the low pulse, or one, three, or five times to the high pulse
R
and their Rif mutants in their respective media and growth conditions. (3.6, 10.8, or 18.0 J/cm2, respectively). Three parallels of both treated
samples and untreated controls were produced for each experiment, (Dansensor, Ringsted, Denmark). The top films of the trays used for
and the experiments were repeated three times on different days. oxygen analysis were also evaluated for structural damages by UV light
For ESBL-producing E. coli and C. divergens, UV light treatments by scanning electron microscopy, where the samples were mounted on
were also performed under modified atmosphere conditions as follows: an aluminum stub using double-sided tape coated with carbon, before
Chicken sample with inoculated bacteria placed in a tray was packaged being coated with gold/palladium using a SC7640 auto/manual high
using a Polimoon 511VG tray sealing machine (RPC Promens AS, Kris- resolution sputter coater (Quorum Technologies, Ashford, UK). An
tiansand, Norway) and UV permeable top film with 65 mm thickness EVO-50-EP environmental scanning electron microscope (Zeiss, Cam-
and an ethylene vinyl alcohol (EVOH) barrier layer (Opalen 65, Bemis, bridge, UK) was used to study the samples at a magnification of
Oshkosh, WI). A gas mixture of 60% CO2 and 40% N2 (AGA, Oslo, Nor- 80003.
way) was used for the packages. The film had an oxygen transmission
rate (OTR) of 5 ml/m2/24 hr/atm at 238C/50% RH, and the trays of 2.5 | Preparation of chicken samples for sensory
dimension 208 3 146 3 32 mm had a barrier layer of high density analyses
polyethylene (HDPE; RPC Promens 528) with an OTR of 3.5 ml/m2/24
Refrigerated fresh skinless chicken breast fillets obtained from a local
hr/atm at 238C/50% RH. Intact packages (MAP-chicken) were exposed
producer were mixed to achieve an equal number of cfu per cm2 on
to UV light doses similar to the chicken samples treated in air (unpack-
the surface. One set of chicken samples were exposed to UV light in
aged chicken), allowing for comparison of bacterial reduction between
air (unpackaged chicken), and were thereafter packaged in modified
the two. Three parallels of both treated samples and untreated controls
atmosphere, while a parallel set of chicken samples were exposed to
were produced for each experiment. The experiments were repeated
UV light under modified atmosphere (MAP-chicken), as described
three times on different days.
above. None of these chicken samples were inoculated with bacterial
Temperatures were measured using a Raynger MX infrared ther-
culture, and both sample sets were then stored at 48C for 6 days
mometer (Raytek Corporation, Santa Cruz, CA). Samples were sub-
before being used for the sensory analyses described below. The color
jected to microbial and physiochemical analyses as described below.
stability of the chicken fillets were evaluated by visual inspection of the
The experiments with pathogens were performed in a Biosafety level 3
chicken before and after UV light exposure, and after storage.
pilot plant.
2.6 | Sensory evaluations

2.3 | Microbial analyses
Descriptive sensory profiling was conducted by a trained sensory panel
Chicken samples were added 90 ml of peptone water and the samples
of 10 assessors at Nofima AS, Norway, according to Generic Descrip-
were homogenized for 1 min in a stomacher (AES Smasher, AES Chem-
tive Analysis (Lawless & Heymann, 2010). All panelists were selected
unex, Bruz, France). Serial 10-fold dilutions from each sample were pre-
2 and trained in accordance with ISO 8586:2012 (International Organisa-
pared. Quantification of C. divergens (cfu/cm ) was performed using a
tion for Standardisation, 2007). The following chicken samples treated
Whitley Automatic Spiral Plater (Don Whitley Scientific, Ltd., West
in air and under modified atmosphere were prepared: untreated
Yorkshire, UK) on cMRS agar (Oxoid) with 200 mg/ml rifampicin (48 hr
control, chicken exposed to UV-C at fluence 0.1 J/cm2 (10 s at
incubation, 308C), ESBL-producing E. coli on BHI (Oxoid) with 50 mg/ml
10 mW/cm2), chicken exposed to UV-C at fluence 0.6 J/cm2 (60 s at
ampicillin (16 hr incubation, 378C), and tryptic soy agar (TSA, Oxoid)
10 mW/cm2), chicken exposed to pulsed UV light at low intensity at
with 200 mg/ml rifampicin was used for Pseudomonas spp. (16 hr incu-
fluence 1.25 J/cm2 and chicken exposed to pulsed UV light three times
bation, 308C), B. thermospacta (48 hr incubation, 308C), S. Enteritidis,
at high intensity giving a fluence of 10.8 J/cm2. Based on a pretrial per-
L. monocytogenes, S. aureus, and EHEC (16 hr incubation, 378C). The
formed by the panelists, a consensus list of attributes for the profiling
number of colonies were determined using an automatic plate reader,
was developed: Smell of raw chicken (sour odor, sunburnt odor, burnt
and the detection limit was 20 cfu/cm2. Since rifampicin resistant
odor, metallic odor, sulfur odor, off-odor, cloying odor, and rancid odor)
strains were used, the indigenous background flora on the chicken was
and odor/taste/flavor of cooked chicken (sunburnt odor, burnt odor,
negligible.
sour flavor, burned flavor, metallic flavor, off-flavor, cloying flavor, and
rancid flavor). Both raw and cooked chicken fillet samples were eval-
2.4 | Packaging film analyses
uated. For the raw samples, the panelists were given 1/6 raw chicken
The UV permeable top film Opalen 65 was evaluated for its ability to fillet served at room temperature on white plastic cups coded by ran-
transmit UV light by measuring UV light at 254 nm (described above). dom three-digit numbers. The cooked samples were heated (1008C,
The extended O2 barrier properties of the top film was evaluated by 100% steam, 30 min) in an Electrolux Air-o-steam oven (Combi LW 6
using empty packages with 100% N2 that were initially exposed to four GN 1/1 Gas) to a core temperature of 788C 6 38C. After heating, the
different UV-C and pulsed UV light treatments up to 10.8 J/cm2 in samples rested for 5 min before each panelist were served one-fourth
addition to an untreated control, with five packages per treatment. The cooked chicken fillet in a white porcelain bowl with lid marked with a
packages were analyzed for concentrations of residual oxygen at pack- random three-digit number, that had been preheated at 658C. Samples
aging and after 21 days of storage with a Dansensor Checkmate 3 were kept at 658C for the evaluation. The panelists had unsalted
crackers and lukewarm water for rinsing the palate between samples. and the selected major compounds (80–100%) on a peak area basis
The coded samples were evaluated in duplicate and served randomized were included in the data analysis.
according to sample, panelist, and replicate. Each panelist recorded
their results at individual speed using an unstructured line scale with 2.8 | Statistical analysis
labeled endpoints ranging from no intensity (1), to high intensity (9),
Bacterial reductions log cfu/cm2 between control and UV light treated
using the EyeQuestion Software (Logic8 BV, Elst, The Netherlands) for
samples were calculated. Analysis of variance (ANOVA) and Tukey’s
direct recording of data.
multiple comparison test were used to determine statistically significant
Changes in the quality or sensory properties of raw chicken as a
effects on the reduction by the treatments (R 3.3.2; R Core Team
result of UV light exposure were also assessed by a smaller consumer
[2016]) using a significance level of .05. For sensory evaluation, the
test. Twenty randomly chosen test persons were asked if they would
same analyses were performed on the descriptive sensory data from
want to use the chicken samples for dinner. In addition, they assessed
the trained panel to identify sensory attributes that discriminated
the quality of the chicken on a scale ranging from very bad (1), to very
between samples.
good (9).
2.7 | Dynamic headspace gas chromatography mass 2.9 | Weibull models

spectrometry For each species, a two-parameter Weibull distribution was fitted to
the observed log reductions to produce predictive models of the
The same set of raw chicken samples used in the pretrail sensory evalu-
effects of UV exposure. The chosen Weibull model is defined as:
ation was subjected to dynamic headspace gas chromatography mass
b
spectrometry (GC/MS) analysis. Based on variation found both in the N 21 f
log10 5 ;
sensory results and the GC/MS results of the pretrial, chicken samples N0 loge ð10Þ a
that showed the greatest variation were further selected for analysis of where N0 and N denote the number of bacteria per square cm before
volatile organic compounds. These included: untreated control, chicken and after UV exposure, respectively, f is the UV dose (fluence), a is the
exposed to UV-C light at fluence 0.60 J/cm2 (60 s at 10 mW/cm2) and scale parameter (describes how sharply the curve drops in the begin-
pulsed UV light three times at high intensity giving a fluence of 10.8 J/ ning), and b is the shape parameter (describes the shape of the curve).
cm2 treated in air, and pulsed UV light at low intensity at fluence 1.25 Common models were produced based on log reduction data for all the
J/cm2 treated under modified atmosphere. A gas chromatography anal- bacterial species.
ysis was carried out on chicken samples as previously described (Olsen,
Vogt, Veberg, Ekeberg, & Nilsson, 2005). Fifteen gram aliquots of
3 | RESULTS
homogenized sample (the samples were analyzed in duplicate) were
distributed evenly in 250 ml Erlenmeyer flasks. The samples were
3.1 | Bacterial reductions on skinless chicken fillets
heated to 708C in a water bath and purged with 100 ml/min nitrogen
through a Drechsel-head for 30 min. Volatile compounds were We investigated the effect of UV-C and pulsed UV light against microbial
adsorbed on Tenax GR (mesh size 60/80). Water was removed from flora associated with fresh, skinless chicken fillets. An overview of the
the tubes by nitrogen flushing (50 ml/min) for 5 min in the opposite experimental set-up is shown in Figure 1. Resulting bacterial log reduc-
direction of sampling. Trapped compounds were desorbed at 2508C for tions cfu/cm2 of the food pathogens S. Enteritidis, L. monocytogenes,
5 min in a Perkin Elmer Automatic Thermal Desorption System S. aureus and EHEC, and chicken spoilage bacteria Pseudomonas spp.,
ATD400 and transferred to an Agilent 6890 GC System with an Agilent B. thermospacta, C. divergens, and ESBL-producing E. coli applied to
5973 Mass selective detector, which is a quadrupole, operated in elec- chicken meat surface are shown in Figures 2 and 3 and Supporting
tron impact (EI) mode at 70 eV. The scan range was from 33 to 300 Information Table S1.
amu. The compounds were separated on a DB-WAXetr column from UV-C light exposure with fluences from 0.05 to 3.0 J/cm2 (10
J&W Scientific/Agilent (0.25 mm i.d., 0.5 lm film, 30 m). Helium mW/cm2, from 5 to 300 s) in air, gave the largest reduction of 2.8 log
(99.9999%) was used as carrier gas. The temperature program started for C. divergens after the highest fluence treatment, while only 1.7 log
at 308C for 10 min, increased 18C/min to 408C, 38C/min to 708C, reduction was obtained for EHEC. The lowest fluence level gave up to
6.58C/min to 1608C, and 208C/min to 2308C with a final hold time of 4 2.2 log reduction for S. aureus, and EHEC was reduced the least with
min. Integration of peaks and tentative identification of compounds 1.1 log. By comparing UV-C light results using ANOVA within each
were performed with HP Chemstation (G1701CA version C.00.00, species, some of the shorter treatments were considered statistically
Agilent Technologies, Santa Clara, CA, USA), Wiley 130 KMass Spectral different from the treatments of longer duration for S. Enteritidis
and NIST98 Mass Spectral. Comparison of retention times and mass (Figure 2a, range 1.6–2.4 log), Pseudomonas spp. (2e, 2.0–2.7 log),
spectra of the sample peaks with those of pure standards confirmed C. divergens (2g, 1.9–2.8 log), and ESBL-producing E. coli (2h, 1.7–2.8
identities of several of the components. Heptanoic acid ethyl ester was log), while none of the treatments were statistically different from each
used as internal standard. System performance was checked with other for L. monocytogenes (2b, 1.5–1.8 log), S. aureus (2c, 2.2–2.6 log),
blanks and standard samples before, during and after the sample series, EHEC (2d, 1.1–1.7 log), and B. thermospacta (2f, 1.7–2.7 log).
(a) Skinless chicken (b)

Skinless chicken
fillets inoculated with fillets with no added
bacteria bacteria
Pseudomonas spp. C. divergens

SPOILAGE
B. Thermospacta E. coli ESBL
C. divergens
E. coli ESBL
Unpackaged MAP
PATHOGENIC
S. Enteridis
L. monocytogenes
S. aureus
E. coli EHEC
UV light treatments
Unpackaged MAP
Descripve Analysis of
UV light treatments sensory volale
profiling compounds
Bacterial reducon
aer exposure
F I G U R E 1 Flowchart illustrating the experimental set-up. Reduction of bacteria on skinless chicken fillets using UV light treatments (a), and
sensory analyses of chicken fillets treated with UV light (b). Chicken fillets inoculated with pathogens and bacteria often found as natural
contaminants on fresh chicken meat were exposed to different UV light treatments in air, representing unpackaged chicken, and for two
selected species on modified atmosphere packaged (MAP)-chicken. The bacterial species are listed in Table 1. Sensory analyses of chicken
fillets with no added bacteria were conducted after UV light treatments of both unpackaged chicken and MAP-chicken
Sensitivities against pulsed UV light, where fluences from 1.25 to stored under an anaerobic atmosphere with 60% CO2 and 40% N2,
18.0 J/cm2 were used, seemed to be more similar between the differ- and the UV permeable top film allowed for UV light exposure of intact
ent species than for UV-C light. Reductions after pulsed UV light expo- packages. C. divergens reduction after UV-C light treatments ranged
2
sure in air at the highest fluences (10.8 and 18.0 J/cm ) ranged from from 1.3 to 1.8 log, and after pulsed UV light treatments from 0.5 to
1.6 log for L. monocytogenes and C. divergens to 3.0 log for S. aureus, 1.5 log. The UV-C light treatments at the lowest fluences (0.05, 0.1, 0.3
Pseudomonas spp. and B. thermospacta. For the low fluence exposure J/cm2) resulted in approximately 0.7 log lower reduction on MAP-
of 1.25 J/cm2, reductions ranged from 0.9 log for S. Enteritidis to 1.7 chicken compared with unpackaged chicken, and 1.4 log lower reduc-
log for Pseudomonas spp. ANOVA on the pulsed UV light results within tion was seen for the highest fluence treatment (3.0 J/cm2). ANOVA
each species defined the treatment at low fluence statistically different on the UV-C light results confirmed the observed differences statisti-
from some or all of the higher intensity treatments, thus increased cally (results not shown). After pulsed UV light exposure, reductions
reduction was obtained by increasing the UV dose. The range of reduc- were similar for MAP-chicken and unpackaged chicken samples for the
tion was 0.9–2.4 log for S. Enteritidis (Figure 2a), 1.1–2.0 log for highest fluences (10.8 and 18.0 J/cm2), while for fluences of 1.25 and
L. monocytogenes (2b), 1.3–3.0 log for S. aureus (2c), 1.1–2.9 log for 3.6 J/cm2, 0.9 and 0.7 log lower reductions, respectively, were seen on
EHEC (2d), 1.7–3.0 log for Pseudomonas spp. (2e), 1.3–3.0 log for B. MAP-chicken, which were confirmed statistically by ANOVA (not
thermospacta (2f), and 1.3–2.8 log for ESBL-producing E. coli (2h). C. shown). Reduction of ESBL-producing E. coli after UV-C light treat-
divergens deviated from this pattern, for which none of the treatments ments ranged from 1.5 to 2.5 log, and after pulsed UV light treatments
were considered statistically different from each other and reductions from 0.6 to 1.7 log. ANOVA on the UV-C light results confirmed statis-
ranged from 1.5 to 1.8 log (Figure 2g). tically that reductions on MAP-chicken and unpackaged chicken sam-
In the in vitro illumination experiments of petri dishes, the UV light ples were similar (not shown). For pulsed UV light, lower reductions
treatments inactivated all the bacterial species by 5–7 log, except from were seen for the MAP-chicken samples regardless of UV dose, 0.7,
L. monocytogenes that was able to withstand the low fluence 1.25 J/ 1.1, 0.9, and 1.3 log lower reductions for fluences of 1.25, 3.6, 10.8,
2
cm treatment with pulsed UV light better than the other species, and 18.0 J/cm2, respectively, confirmed statistically by ANOVA (not
showing approximately 4 log reduction (not shown). shown).
Bacterial reductions after exposure with UV-C and pulsed UV light The applied UV light up to 10.8 J/cm2 did not impair the oxygen
against C. divergens and ESBL-producing E. coli on MAP-chicken, are barrier properties and structural integrity of the UV permeable top film,
shown in Figure 3 and Supporting Information Table S1. Samples were and the O2 concentrations of the trays increased from approximately
(a) S. Enteritidis (b) L. monocytogenes (c) S. aureus (d) E. coli EHEC
Bacterial reduction (log CFU/cm2)
Fluence (J/cm2)
(e) Pseudomonas spp. (f) B. thermospacta (g) C. divergens (h) E. coli ESBL
Fluence (J/cm2)
F I G U R E 2 Reductions of (a) S. Enteritidis, (b) L. monocytogenes, (c) S. aureus, (d) enterohemorrhagic E. coli (EHEC), (e) Pseudomonas spp., (f)
B. thermospacta, (g) C. divergens, and (h) ESBL-producing E. coli on chicken fillet meat after continuous UV-C (white bars) and pulsed UV light
(grey bars) exposures at different fluences (J/cm2). The chicken samples were treated in air, representing unpackaged chicken. Three sepa-
rate ANOVA were performed for each species, represented by upper case letters (comparing UV-C and pulsed UV light treatments), num-
bers (comparing UV-C light treatments) and lower case letters (comparing pulsed UV light treatments). Samples containing the same letter/
number were not considered different
0.12 6 0.03% at packaging to 0.69 6 0.02% after 21 days, and were values were less than 1, the Weibull fits of the reduction data were
similar for the different UV light treatments and the untreated control. concave upward. The highest ß values were obtained for EHEC and
Scanning electron microscopy analysis showed no structural damages S. Enteritidis (0.32 and 0.31, respectively) for pulsed UV light. The a
to the UV treated films (not shown). The ability of the film to transmit (scale parameter) values were very small, implying concentrated dis-
UV light was measured as 80.5% at 254 nm, which was compensated tribution, as seen by how sharp the curve drops in the beginning.
for by increasing the UV doses accordingly in the illumination There was a noticeable difference between the two UV methods,
experiments. where higher a values were obtained for UV-C light than for pulsed
UV light, with C. divergens as an exception. Common models based
3.2 | Weibull models describing bacterial reduction on log reduction values for all the species gave a good fit for the
majority of the species, but for L. monocytogenes exposed to both
Weibull models created to predict the log reduction patterns for the
UV-C and pulsed UV light, reduction was overestimated. The same
different bacterial species are shown in Figure 4 and parameters for
was seen for EHEC exposed to UV-C light and C. divergens exposed
the models are listed in Table 2. RMSE values indicating the good-
to pulsed UV light.
ness of fit, were the lowest for S. aureus exposed to UV-C light
(0.20) and the highest for Pseudomonas spp. exposed to pulsed UV
3.3 | Sensory evaluation of UV light treated chicken
light (0.55). Determination coefficient (R2) values ranged from 0.41
to 0.80 for UV-C light and from 0.47 to 0.89 for pulsed UV light. Changes in quality or sensory properties of chicken fillets as a result
Since R2 indicates the proportion of variation in log reduction of UV light treatments were assessed by 10 trained assessors. Their
explained by the fitted Weibull model, a value approaching 1 would evaluation results are shown in Figure 5, where raw chicken samples
signify perfect predictability. Since all of the ß (shape parameter) were evaluated for odor and cooked chicken samples for odor/
(a) C. divergens (b) E. coli ESBL T AB LE 2 Parameters for Weibull models predicting bacterial reduc-
tion on chicken fillet meat after continuous UV-C and pulsed UV
3.5
3.0 light exposures, and goodness-of-fit parameters of the models
A
1
AB Bacterial species a b RMSE R2
AC 1
2.5
12
A
1 ACD
Continuous E. coli EHEC 2.03E-06 0.09 0.31 .75
ACD
2.0
AB
AC
12 a BCD UV-C light L. monocytogenes 2.02E-09 0.07 0.47 .41
1 AB CE ab
AC ab
AC AC 1
a 2 S. Enteritidis 2.35E-05 0.14 0.41 .64
1.5
1 1 DE
BC bc S. aureus 2.22E-15 0.05 0.20 .76
ab
Pseudomonas spp. 2.86E-09 0.09 0.39 .68
1.0
C E
b c
C. divergens 1.45E-08 0.10 0.37 .74
0.5
B. thermospacta 1.66E-07 0.11 0.31 .80

E. coli ESBL 1.65E-08 0.10 0.38 .74
0.0
All 9.89E-09 0.09 0.53 .25

0.05
1.25
0.05
1.25
0.1
0.3
0.6
3.0
3.6
10.8
18.0
0.1
0.3
0.6
3.0
3.6
10.8
18.0
Pulsed C. divergens 3.79E-10 0.06 0.29 .86
Fluence (J/cm2) UV light L. monocytogenes 2.27E-04 0.13 0.37 .63
S. Enteritidis 6.32E-02 0.31 0.42 .79
E. coli EHEC 5.29E-02 0.32 0.41 .79
FIGURE 3 Reductions of (a) C. divergens and (b) ESBL-producing
E. coli ESBL 7.58E-03 0.24 0.28 .89
E. coli on MAP-chicken exposed to continuous UV-C (white bars) Pseudomonas spp. 1.31E-03 0.20 0.55 .71
and pulsed UV light (grey bars) at different fluences (J/cm2). A gas S. aureus 6.61E-03 0.24 0.47 .47
mixture of 60% CO2 and 40% N2 and a UV permeable top film was B. thermospacta 9.21E-03 0.26 0.37 .82
used for the packages. Three separate ANOVA were performed for All 6.23E-03 0.22 0.54 .46
each species, represented by upper case letters (comparing UV-C
and pulsed UV light treatments), numbers (comparing UV-C light
treatments) and lower case letters (comparing pulsed UV light Denaturation of proteins in chicken has been considered to be
treatments). Samples containing the same letter/number were not initiated at temperatures higher than 568C (Murphy, Marks, &
considered different Marcy, 1998). Only minor elevation of the temperature was
observed, 2.5–4.08C and 4.0–6.58C for UV-C light treatments at flu-
taste/flavor. A statistically significant difference between the sam- ences 0.6 J/cm2 and 3.0 J/cm2, respectively, and 0.5–2.58C and
ples was only registered for the odor characterized as sunburnt 2.5–3.58C for pulsed UV light treatments at fluences 10.8 and 18.0
(p < .001), which is associated with that of sunburnt human skin. J/cm2, respectively. The rise in surface temperature was only tem-
Most notably, treatment with the highest dose of pulsed UV light porary since the surface was rapidly cooled by the low temperature
(10.8 J/cm2) in air gave the highest intensity of the sunburnt odor of the interior of the chicken fillet.
(sensory intensity value score of 3.4). After cooking, this effect of
the UV light treatment could not be detected. From the consumer
3.4 | Volatile organic compounds
test, UV light exposed raw chicken fillet samples assessed by 20 ran-
dom consumers could not be differentiated from untreated control Nearly 100 different volatile organic compounds were detected by
samples (data not shown). By visual inspection, the color stability dynamic headspace/GC-MS in the raw chicken samples that were ana-
was not affected by the treatments at the doses used (data not lyzed, of which approximately 70 compounds could be identified. The
shown). major compounds were ketones (C2–C5, C7), alcohols (C2–C8), acids
0.0 0.5 1.0 1.5 2.0 2.5 3.0 0 3 6 9 12 15 18

0.0
0.0
CFU/cm2)
−1.0
−1.0
Bacterial reduction (log
E. coli EHEC
L. monocytogenes C. divergens
−2.0
−2.0
L. monocytogenes
S. Enteritidis
S. aureus
S. Enteritidis
Pseudomonas spp.
C. divergens E. coli EHEC
−3.0
−3.0
B. thermospacta E. coli ESBL

E. coli ESBL Pseudomonas spp.
S. aureus
F l u e n c e ( J / c m 2) F l u e n c e ( J / c m 2) B. thermospacta
(a) (b)
F I G U R E 4 Weibull models for bacterial log reduction as a function of UV exposure. Models for each species (black continuous line) and
common models (red dotted line) are shown for bacterial reduction on unpackaged chicken fillet meat after (a) continuous UV-C and (b)
pulsed UV light exposures at different fluences (J/cm2)
4
A A AA AAAAAAAAAA
BBB B BBBB
AAAAAAAAAA AAAAAAAAAA
CCC CCC C C
Intensity
3 AAAAAAAAAA
AAAAAAAAAA
2
AAAAAAAAAA
AAAAAAAAAA
1
Sour Sunburnt Burnt Metallic Sulfur Off- Cloying Rancid
(a) odour odour odour odour odour odour odour odour
AAAAAAAAAA
4
AAAAAAAAAA AAAAAAAAAA
A A A A A A AA A A
AAAAAAAAAA
Intensity
2
AAAAAAAAAA
AAAAAAAAAA
AAAAAAAAAA
1
Sunburnt Burnt Sour Burnt Metallic Off- Cloying Rancid
(b) odour odour flavour flavour flavour flavour flavour flavour
Untreated-CO2:N2 Untreated-O2 PUV-Hx3-CO2:N2 PUV-Hx3-O2 PUV-L-CO2:N2

PUV-L-O2 UVC-10-CO2:N2 UVC-10-O2 UVC-60-CO2:N2 UVC-60-O2
F I G U R E 5 Sensory analysis of (a) raw chicken fillet samples and (b) cooked chicken fillet samples. Chicken samples were exposed to
continuous UV-C light at 10 mW/cm2 for 10 s (UVC-10) and 60 s (UVC-60), giving fluences of 0.1 J/cm2 and 0.60 J/cm2, respectively, and
pulsed UV light to a low pulse with fluence of 1.25 J/cm2 (PUV-L) and three times to a high pulse giving a fluence of 10.8 J/cm2 (PUV-
Hx3), both in air (O2) and anaerobic (CO2 : N2) atmospheres, representing unpackaged chicken and MAP-chicken, respectively. The inten-
sities of different odors of raw samples and odor/taste/flavor of cooked samples were registered, 1 5 no intensity and 9 5 high intensity.
The letters above the columns indicate grouping according to ANOVA and Tukey multiple comparison test. Samples with the same letter
are considered being equal for the specific property
(C2–C7), fatty and nonfatty aldehydes (C2–C9), hydrocarbons (C5–C7), follows: dimethyltrisulfide r 5 .70 (p < .01), 2-pentanone r 5 .95
and sulfides. Only a few compounds were observed to increase in con- (p < .0025), 1-pentanol r 5 .91 (p < .005), pentane (r 5 .92, p < .005),
centration as a result of exposure to UV light. This included dimethyltri- heptane (r 5 .81, p < .01), propanoic acid (r 5 .98, p < .001), and hexanal
sulfide, pentane, heptane, propanoic acid, 2-pentanone, 1-pentanol, (r 5 .81, p < .01). The sample in which all the compounds increased the
and hexanal (Figure 6). Linear correlation with the odor scores were most, was chicken exposed to pulsed UV light at fluence 10.8 J/cm2
calculated, and gave correlations with the sunburnt odor scores as treated in air.
fluence was employed for the two methods, which can be explained by
Hexanal
most of the energy being emitted at 254 nm, where the germicidal
effect is close to the maximum (Bintsis et al., 2000).
1-Pentanol
In the range tested, a limited dose-response effect was observed,
2-Pentanone likely caused by shading effects of the irregular surface structure of the
chicken fillet. The increase in reduction with increasing dose was
Propanoic acid though more apparent for the pulsed UV light. Any substance between
the light source and the bacterium that absorbs light will impair the
Heptane decontamination process (Gomez-Lopez et al., 2007). Even when a sur-
face appears smooth to the naked eye, it may harbor crevices and
Pentane
cracks where bacteria are shielded against direct exposure, and bacteria
may also be covered by protein or other organic matrices. Moreover,
Dimethyltrisulfide
the average size of a bacterium is approximately 1 mm 3 2 mm, and
0 50 100 150 200 250 300 350 although its spreading was carried out carefully, it is practically impossi-
pg/g ble to avoid some overlapping. A shielding effect for colonies of
L. monocytogenes growing on petri dishes where the upper cells of a
PUV-Hx3-O2 UVC-60-O2 Untreated-O2 PUV-L-CO2:N2 colony appeared to protect the lower cells has previously been
described (Gomez-Lopez et al., 2005). At high fluence rates, the light
FIGURE 6 Volatile organic compounds from chicken which
should be able to penetrate deeper, but still, the efficiency of using UV
showed an increase in concentration (pg/g) as a result of exposure
light for decontamination of foods is lower than when tested on
to UV light. The samples included were chicken exposed to pulsed
UV light at low intensity at fluence 1.25 J/cm2 (PUV-L) treated smooth surfaces. Reductions of 5–7 log achieved on agar in petri
under anaerobic (CO2:N2) atmosphere (MAP-chicken), an untreated dishes was in accordance with previous reports (Farrell et al., 2010;
control (Untreated), chicken exposed to UV-C light at 10 mW/cm2 Gomez-Lopez et al., 2005; Paskeviciute et al., 2011; Rowan et al.,
for 60 s (UVC-60) giving a fluence of 0.60 J/cm2 and pulsed UV 1999), and the observed higher resistance of L. monocytogenes to
light three times at high intensity (PUV-Hx3) giving a fluence of
pulsed UV light, reduced only 4 log after treatment at low fluence of
10.8 J/cm2 treated in air (O2). The precision of replicate measure-
ments were within 15% 1.25 J/cm2, has also been reported previously (Gomez-Lopez et al.,
2005; Lasagabaster & de Maranon, 2012). In general, the reductions of
4 | DISCUSSION inoculated bacteria on chicken fillet surface observed in this study cor-
related well with previous findings, both for UV-C (Chun et al., 2010;
4.1 | Effect of UV treatment on inoculated bacteria Haughton et al., 2011a; Isohanni & Lyhs, 2009; Sommers et al., 2016)
and for pulsed UV light (Keklik et al., 2010; Paskeviciute et al., 2011),
There are large differences between the conventional continuous UV-
including for C. divergens, Pseudomonas spp., and B. thermospacta, for
C light and pulsed UV light with respect to wavelengths, intensities,
which previous reports on UV light inactivation on food surfaces does
and exposure times. In this work, we have compared the efficacy of
not exist or are scarce. EHEC seemed to resist the UV-C light treat-
continuous UV-C light and pulsed UV light in reducing bacteria on
ments better than ESBL-producing E. coli, and better than the other
chicken fillet. We used multi strain mixtures of the same species and
species tested as well.
bacterial cells that were in the same state during the different treat-
The Weibull distribution is suitable for the analysis of bacterial
ments. In earlier studies, single strains were often used which may not reduction (Chen, 2007; Keklik, Demirci, Puri, & Heinemann, 2012;
show reductions representative for the species. Differences in reduc- Martin et al., 2007; Ugarte-Romero, Feng, Martin, Cadwallader, &
tion within species have been reported, and state of the cells can influ- Robinson, 2006; van Boekel, 2002), and was previously demonstrated to
ence the sensitivity to UV light (Farrell et al., 2010; Haughton et al., be more successful than models such as the log-linear model and first-
2011b). To avoid possible changes in sensory perception, it is desirable order kinetic model (Chen, 2007; Keklik, Demirci, et al., 2012; Martin
to maximize bacterial reduction without treating the surface of a prod- et al., 2007). The model seemed to be a useful tool to describe the
uct more than necessary. Treatment levels employed for both UV reduction patterns and give clues to how pathogens and spoilage bacte-
methods were practical and relevant within industrial production, from ria on chicken fillet surfaces are likely to respond to UV light treatments.
weak exposures resulting in limited bacterial reduction, up to levels The Weibull fits of the reduction data were concave upward, indicating
exceeding the maximum permitted dose by the FDA for pulsed UV that exposed cells were destroyed and that the more resistant cells or
light (FDA, 2010). The fluences are not directly comparable between those shaded from exposure were left undamaged.
the two methods, since the different wavelengths in the UV spectrum To our knowledge, studies on UV light treatment of intact pack-
have different germicidal effectiveness (Bintsis, Litopoulou-Tzanetaki, ages of MAP-chicken fillet for reducing bacteria on the chicken surface
& Robinson, 2000). For UV-C exposure at 0.05 J/cm2, the germicidal have previously not been reported. UV light reduction of bacteria on
effect was comparable to a fluence of 1.25 J/cm2 for the pulsed UV various packaging materials have, however, been studied (Haughton
light. UV-C light showed a higher germicidal effect when the same et al., 2011b), and vacuum-packaged chicken breast inoculated with
Salmonella Typhimurium treated with pulsed UV light were shown to exposure per area compared to our applied UV doses, thus the results
give about 2 log reduction, but with double the exposure time (30 s) in may not be directly comparable. Paskeviciute et al. (2011) investigated
comparison with unpackaged samples (15 s) (Keklik et al., 2010). The chemical changes in pulsed UV light treated chicken breasts, and
additional bacterial reduction obtained on ready packaged chicken fillet reported that the intensity of lipid peroxidation in control and treated
product would increase shelf life and safety. Treatment after packaging chicken samples differed in 0.16 mg malondialdehyde per kilogram of
should be simple to implement at industrial packaging lines without chicken meat. However, taste panelists did not observe any changes in
reductions in production efficiency. organoleptic properties of treated raw chicken, chicken broth or
cooked chicken meat in comparison with control. Although treated raw
4.2 | Sensory quality of the chicken fillets chicken samples could not be differentiated from an untreated control
sample by the 20 random chosen consumers in the present study,
Meat exposed to UV light can develop off-flavors caused by the
more extensive consumer studies could aid in determining whether
absorption of ozone and oxides of nitrogen, or because of photochemi-
such UV light treatments are acceptable.
cal effects on the lipid fractions of the meat (Bintsis et al., 2000). Lipid
The color of raw or cooked poultry meat is by origin pale with a
oxidative rancidity is regarded as the most important nonmicrobial fac-
low content of the muscle pigment myoglobin. Furthermore, the color
tor responsible for meat deterioration, resulting in adverse changes in
of raw meat is dependent on the oxidation state of myoglobin (Mugler
appearance, texture, odor, and flavor (Frankel, 1998). An increase in
& Cunningham, 1972; United States Department of Agriculture, 2013).
fatty aldehydes due to lipid oxidation during irradiation of poultry meat
Chicken breasts exposed to high doses of UV light was previously
has been documented (Du, Ahn, Nam, & Sell, 2000, 2001; Du, Hur,
reported to turn darker, show more redness and a slight increasing
Nam, Ismail, & Ahn, 2001; Kim, Nam, & Ahn, 2002). The major fatty
amount of yellow coloration (Park & Ha, 2015). The color of the
aldehyde hexanal is a typical volatile secondary lipid oxidation product
chicken fillets was not affected by the treatments at the doses used in
(Beltran, Pla, Yuste, & Mor-Mur, 2003; Jayasena, Ahn, Nam, & Jo,
our experiments, as in agreement with other reports (Chun et al., 2010;
2013; Shi & Ho, 1994). Although we observed an increase in the con-
Haughton et al., 2011a). Together these results indicate that sensory
centration of hexanal, particularly for unpackaged chicken exposed to
and quality changes are small or negligible both after UV-C and pulsed
UV light, no significant effect was found on the corresponding rancid-
UV light treatments.
related sensory attributes in the professional sensory evaluation. This
suggests that lipid oxidation does not have a negative impact on the
4.3 | Advantages and disadvantages of continuous
perceived odor and flavor of the chicken meat at the applied UV doses.
UV-C and pulsed UV treatments
The higher intensity of the sunburnt odor for chicken exposed to the
most intense dose of pulsed UV light, does, however, seem to pose Both UV-C and pulsed UV light treatments provide effective tools for
restrictions on the upper limit of treatment of unpackaged chicken. The reduction of microorganisms. They are rapid and efficient nonchemical,
sensory intensity value was though only 3.4, which is considered rela- nonionizing, and nonthermal surface decontamination treatments and
tively low, and for lower doses relevant in industrial application, the can be used in continuous processing. The methods have been shown as
odor should not be a problem. Detected changes in concentrations of effective technologies for decontamination of stainless steel conveyors
volatile compounds correlated well with the sensory observations. and surfaces in the production environment (Haughton et al., 2011b;
Increased levels were seen in unpackaged chicken after UV light expo- Sommers, Sites, & Musgrove, 2010). They can be used on foods and
sure. Hydrocarbons may be generated during irradiation of poultry synergistically with other treatments (Mukhopadhyay & Ramaswamy,
meat (Du, Ahn, et al., 2000, 2001; Du, Hur, et al., 2001; Kim et al., 2012). The methods require little energy use, are easy to implement
2002), where increased concentrations of propanol and butanol have and require no increase in work load. UV light is safe to apply, but
been documented (Du et al., 2000, 2001; Du, Hur, et al., 2001). In some precautions have to be taken to avoid exposure of workers to
accordance, we detected increased levels of pentane, heptane and 1- light and to evacuate any ozone generated by the shorter UV wave-
pentanol. Sulfur compounds with low odor thresholds are important to lengths (Gomez-Lopez et al., 2007). The effect of both UV-C and
odor associated with irradiation (Angelini, Merritt, Mendelsohn, & King, pulsed UV light is impaired in opaque matter, where bacteria are
1975; Batzer & Doty, 1955; Patterson & Stevenson, 1995). Dimethyl- shielded from direct exposure such as by food surface topography,
trisulfide, although only detected in small amounts in unpackaged organic matter, or by other bacteria. The UV light treatments of this
chicken after UV light exposure, was reported by Patterson and Ste- study did not alter the properties of the EVOH film used, as was also
venson (Patterson & Stevenson, 1995) to be the most potent off-odor the case with polyethylene, polypropylene and polyvinyldichloride
compound in irradiated raw chicken. Other compounds that showed an films (Tarek, Rasco, & Sablani, 2015). The top film used transmitted
increase and which character could be associated with sunburnt/irradi- approximately 80% of the UV light, while in previous studies, films
ated odor and flavor, were 2-pentanone (roasted sweet), and 1- with polypropylene and polyethylene barrier layers transmitted 75%
pentanol (roasted meat) (Brewer, 2009). Together these three com- (Keklik, Demirci, & Puri, 2009) and 72% (Keklik et al., 2010), respec-
pounds likely contribute to the sensory perceived sunburnt odor. Irradi- tively, of pulsed UV light at 1.27 J/cm2. By using a packaging film
ation of poultry meat is though based on irradiation by electrons using with a high UV transmission, the chicken fillets could be packaged
an accelerator, representing far higher dose in terms of energy before the UV light treatment, thereby avoiding the risk of
recontamination. Both methods would be beneficial for large scale Anonymous. (2000). Lebensmittelbestrahlungsverordnung vom 14. Dezem-
industrial UV decontamination operations. UV-C light treatment is a ber 2000 (BGBl. I S. 1730), die zuletzt durch Artikel 62 der Verordnung
vom 31. August 2015 (BGBl. I S. 1474) geändert worden ist. Germany.
low cost strategy with low maintenance (Keklik, Krishnamurthy, &
Batzer, O. F., & Doty, D. M. (1955). Nature of undesirable odors formed
Demirci, 2012). The treatment time is somewhat longer in comparison
by gamma irradiation of beef. Journal of Agricultural and Food Chemis-
with pulsed UV light treatment, and therefore the equipment may try, 3(1), 64–67. https://doi.org/10.1021/Jf60047a009
require more space if installed over for example a conveyor belt. Beltran, E., Pla, R., Yuste, J., & Mor-Mur, M. (2003). Lipid oxidation of
Pulsed UV light provides rapid decontamination, but involves equip- pressurized and cooked chicken: Role of sodium chloride and
ment that is more elaborate. The xenon flash lamps used for pulsed mechanical processing on TBARS and hexanal values. Meat Science,
64(1), 19–25. https://doi.org/10.1016/S0309-1740(02)00132-8
UV light are also more environment friendly than the mercury-vapor
Bintsis, T., Litopoulou-Tzanetaki, E., & Robinson, R. K. (2000). Existing
lamps typically used in UV-C light treatment (Gomez-Lopez et al.,
and potential applications of ultraviolet light in the food industry - A
2007). critical review. Journal of the Science of Food and Agriculture, 80,
637–645. https://doi.org/10.1002/(Sici)1097-0010(20000501)
80:6<637::Aid-Jsfa603>3.0.Co;2-1
5 | CONCLUSION
Blom, H., Nerbrink, E., Dainty, R., Hagtvedt, T., Borch, E., Nissen, H., &
Nesbakken, T. (1997). Addition of 2.5% lactate and 0.25% acetate
Despite good hygiene practices during production of fresh meat, con- controls growth of Listeria monocytogenes in vacuum-packed, sen-
tamination of carcasses with pathogens and spoilage bacteria cannot sory-acceptable servelat sausage and cooked ham stored at 4
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Received: 21 June 2017 | Revised: 20 September 2017 | Accepted: 19 October 2017

Chicken fillets subjected to UV-C and pulsed UV light:

Anette McLeod | Kristian Hovde Liland | John-Erik Haugen | Oddvin Sørheim |

Nofima, Norwegian Institute of Food,

ESBL-producing E. coli MF5658 Chickend

2.6 | Sensory evaluations

2.7 | Dynamic headspace gas chromatography mass 2.9 | Weibull models

(a) Skinless chicken (b)

Pseudomonas spp. C. divergens

(a) S. Enteritidis (b) L. monocytogenes (c) S. aureus (d) E. coli EHEC

Bacterial reduction (log CFU/cm2)

B. thermospacta 1.66E-07 0.11 0.31 .80

All 9.89E-09 0.09 0.53 .25

0.0 0.5 1.0 1.5 2.0 2.5 3.0 0 3 6 9 12 15 18

B. thermospacta E. coli ESBL

Untreated-CO2:N2 Untreated-O2 PUV-Hx3-CO2:N2 PUV-Hx3-O2 PUV-L-CO2:N2

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