Food Control 59 (2016) 377e385

Contents lists available at ScienceDirect

Food Control
journal homepage: www.elsevier.com/locate/foodcont

The heterogeneity in the type of shelf life label and storage

instructions on refrigerated foods in supermarkets in Belgium and
illustration of its impact on assessing the Listeria monocytogenes
threshold level of 100 CFU/g
Siele Ceuppens, Sigrid Van Boxstael, Astrid Westyn, Frank Devlieghere,
Mieke Uyttendaele*
Ghent University, Faculty of Bioscience Engineering, Department of Food Safety and Food Quality, Laboratory of Food Microbiology and Food Preservation
(LFMFP), Ghent, Belgium

a r t i c l e i n f o a b s t r a c t

Article history: Confusion about the use of shelf life labels among consumers is a major contributor to avoidable food
Received 26 January 2015 waste at the end of the food supply chain. By means of an inventory snapshot of all pre-packed refrig-
Received in revised form erated food products (n ¼ 1477), including a wide range of fresh-cut vegetables, smoked fish, meat and
25 May 2015
dairy products, from four different supermarket chains in Belgium, the use and consistency in use of shelf
Accepted 2 June 2015
Available online 4 June 2015
life labels (i.e. ‘use by’ and ‘best before’ dates) within food product categories and supermarkets was
investigated. In addition, recommended storage conditions were noted and by means of a challenge test
on a randomly selected cooked pork meat product the impact of storage temperature (4  C, 7  C and
Keywords:
Use by
10  C) and validity of the set shelf life (13 days) and shelf life label (a ‘best before’ date) was evaluated. It
Best before was noted that a mixed use of the ‘use by’ and ‘best before’ dates and recommended storage conditions
Challenge testing occurs in most refrigerated food product categories except for smoked fish for which on all product
Consumer brands (including private labels and premium brands) at all retailers a ‘use by’ data and storage at 4  C
Retail was recommended. The inconsistency of shelf life labels and storage conditions within a food product
category is to some extent expected as product characteristics and packaging and storage conditions will
impact on microbial quality and safety such as growth potential of Listeria monocytogenes. Still a mixed
use will detract from consumers' understanding of the shelf life label and contribute to food waste. In
addition, recommended storage conditions were noted and by means of a challenge test with
L. monocytogenes on a randomly selected cooked pork meat product the impact of storage temperature
(4  C, 7  C and 10  C) and validity of the set shelf life (13 days) and shelf life label (a ‘best before’ date)
was evaluated. Challenge testing indicated substantial growth potential of L. monocytogenes (on
average þ1.0, þ2.0 and þ4.0 log CFU/g respectively at 4, 7 and 10  C) within the set shelf life and also
indicates a potential public health risk if the pathogen would be present, thus indicating the inappro-
priateness of the setting of a ‘best before’ date. This highlights that more attention is needed to reflect, as
an individual company or an industry association or competent authority on more stringent guidelines
on the use and the validation of shelf life labels.
© 2015 Elsevier Ltd. All rights reserved.

1. Introduction the consumer level (Lipinski et al., 2013). Approximately 30% of

In Europe, approximately 100 kg of food is lost or wasted per
capita per year (FAO, 2011). It is estimated that ca 52% is wasted at
* Corresponding author. Coupure Links 653, 9000 Ghent, Belgium.
E-mail address: mieke.uyttendaele@ugent.be (M. Uyttendaele).
food items was discarded by consumers in the UK because the date
of the shelf life label had passed (Lyndhurst, 2011). In Sweden, 9.2%
of all discarded food items were thrown away by the consumers
because the ‘best before’ date had passed, but the actual percentage
may be higher because participants with a higher environmental
consciousness than average were selected for this study (Williams,
Wikstro € m, Otterbring, Lo €fgren, & Gustafsson, 2012). One of the

http://dx.doi.org/10.1016/j.foodcont.2015.06.009
0956-7135/© 2015 Elsevier Ltd. All rights reserved.
378 S. Ceuppens et al. / Food Control 59 (2016) 377e385
many interventions to reduce food waste is to optimize use of shelf
life labels for pre-packed food products (Lipinski et al., 2013). Two
types of shelf life labels are available: the ‘best before’ date and the
‘use by’ date. The ‘best before’ date is a date of minimal durability
which provides the consumer with the period during which the
quality of the product is guaranteed, but it does not mean that the
product is no longer fit for human consumption after this date has
passed (EC, 2000; EC, 2011). As a consequence, food products may
be consumed and sold after the ‘best before’ date if the quality and
the safety of the food product is still acceptable, i.e. in compliance
with the Food Safety Act 1990 and the General Food Regulations
2004 (DEFRA, 2011). For foods which are highly perishable from a
microbiological point of view and are therefore likely to constitute
an immediate danger to human health, the ‘use by’ date indicates
the period during which the safety of the food product is guaran-
teed (DEFRA, 2011; EC, 2000; EC, 2011). After the ‘use by’ date these
products are not meant to be consumed, and thus not to be sold,
because of the risk of foodborne illness. The shelf life labels should
be accompanied with instructions about the storage conditions,
since these greatly influence the shelf life (article 25 in EC, 2011).
Moreover, this EU regulation stipulates that appropriate storage
conditions and/or time limit for consumption after opening the
package should be indicated “where appropriate”. Whether a
product has a ‘use by’ or ‘best before’ label and recommendations
on the expiry date and storage conditions are the decisions of the
food producers alone (in case of premium brands) or in collabo-
ration with the retailers (if products are sold under private label of
the retailer), the food business operator setting the product to the
market being responsible for the safety of their products according
to the EU general food law (EC, 2002).
Unfortunately, not all consumers are aware of the meaning of
these different shelf life labels (Van Boxstael, Devlieghere,
Berkvens, Vermeulen, & Uyttendaele, 2014). The primary strategy
of Belgian consumers (n ¼ 907) to judge the edibility of food
products was sensory evaluation of the odour and the appearance
(82.5%), while checking the shelf life labels ranked only second
(67.5%). Slightly less than half (49.3%) of the Belgian consumers
takes the difference in meaning of ‘use by’ and ‘best before’ dates of
food products into account, which indicates that many consumers
do not (fully) understand these dates (Van Boxstael et al., 2014).
Similarly, only half of consumers in the UK were aware that the
‘best before’ date is a quality guideline and the ‘use by’ date a safety
indicator (Lyndhurst, 2008). This lack of understanding, combined
with other factors such as the tendency to generalize and habitual
behavior, hamper correct use of shelf life labels and may lead to
worrying practices such as consumption of smoked fish and meat
products, which are established to be at risk foods for Listeria
monocytogenes, after the ‘use by’ date by considerable fractions
(14.2% and 23.9%, respectively) of the consumers (Van Boxstael
et al., 2014). The perception of consumers of the freshness and
the healthfulness of a food product decreases as the shelf life label
draws closer and declines further after the date has passed, as
shown by a study with identical yogurts carrying various shelf life
labels (Wansink & Wright, 2006). This study suggests that con-
sumers may be inclined to discard products after their ‘best before’
date based on subjective negative evaluation of the sensory quality
of food and thus this label may contribute to unnecessary food
waste. In conclusion, incorrect interpretation of the shelf life labels
by the consumer thus results in either a potential health problem
(the risk of contracting foodborne illness) or in avoidable food
waste (discarding of safe and edible products).
The aim of this study was to investigate by means of an in-
ventory snapshot of all pre-packed refrigerated food products in
four different supermarket chains in Belgium, the use and consis-
tency in use of shelf life labels (i.e. ‘use by’ and ‘best before’ dates)
and recommended storage conditions. In addition by means of a
challenge test with L. monocytogenes on a random selected pre-
packed cooked sliced pork meat product the impact of recom-
mended (4 and 7  C) and reasonably foreseen (10  C) storage
temperature and validity of the set shelf life duration and label of
this meat product (a ‘best before’ date) was evaluated. Furthermore
the rationale and common approaches in setting shelf life labels are
discussed, partially based on the feedback obtained from the
competent authority, the implicated supermarket chains and
cooked meat product production companies when providing them
the survey results.
2. Materials and methods
2.1. Survey on shelf life label on refrigerated pre-packed food
products in supermarkets
One supermarket of each of four different retailers (two of
Belgian origin and two with non-Belgian but neighboring European
countries' headquarters) which all have a substantial market share
in Belgium was visited in the period SeptembereDecember 2013.
After obtaining permission from the supermarkets' manager, pho-
tographs were taken of several food items on display of a selected
number of defined food categories. Subsequently these photo-
graphs were used to register the type of shelf life label (i.e. ‘use by’
or ‘best before’ date), the expiry date and the recommended storage
conditions (both before and if applicable after opening) as indicated
on the package. The whole set of individual refrigerated food items
with often various premium brands and private label formats
offered by the supermarket were allocated to different food cate-
gories i.e. pre-packed (usually pre-cut) vegetables, smoked salmon,
cooked ham, p^ , other cooked meat products (e.g. sausages with
ate
meat from pork, poultry, turkey, veal or meat loaf), fermented meat
products (e.g. salami), other smoked, cured or dried meat products
(e.g. bacon, prosciutto), yogurt, soft cheeses, hard cheeses and a
ready-to-eat mayonnaise based deli-salads (sandwich spreads)
(Table 1). The proportion of food items carrying a ‘use by’ label in
the different food categories (over all supermarkets) or the latter
proportion over all food categories but calculated for the different
supermarkets were statistically analyzed with the Chi-square test
of independence using the program SPSS 22.0 at a significance level
of 95% (p < 0.05). The p-value of the likelihood ratio was taken and
the Bonferroni correction was applied in case of multiple pairwise
comparisons to consistently obtain a family-wise error rate of 5%.
Furthermore, once the results of the survey of the use of shelf
life labels were available, some feedback was collected on these
findings. Cooked meat products were selected as an illustrative
example in this feedback, and also in the follow-up
L. monocytogenes challenge testing study, to evaluate the rationale
and impact of setting a shelf life label, expiry date and storage
conditions. For this feedback moment an online questionnaire in
SurveyMonkey (https://nl.surveymonkey.com/) was used to con-
sult the quality managers of the four visited supermarket chains as
well as the quality managers of four selected cooked meat pro-
duction companies (two large industrial companies and two SMEs,
all four situated in Belgium) and a representative of the Belgian
Federal Public Service of the Public Health, Food Chain Safety and
Environment.
2.2. Challenge test with L. monocytogenes to evaluate the shelf life
label
A cooked meat product was selected as one relevant food
commodity being an at risk product for L. monocytogenes contam-
ination (EFSA, 2007; Gilbert, McLauchlin, & Velani, 1993), with
 S. Ceuppens et al. / Food Control 59 (2016) 377e385 379

Table 1
Ratio of the number of different refrigerated products in four supermarkets in Belgium from different chains carrying 'use by' dates to the total number of refrigerated food
products offered by these supermarkets (the remaining products carried a 'best before' date). Different letters indicate statistically significant differences of the proportions of
'use by' dates present on food items from all supermarkets combined compared with all different food product categories.

Food product category Supermarket 1 Supermarket 2 Supermarket 3 Supermarket 4 Total %

Smoked salmon 18/18 3/3 5/5 3/3 29/29 100.0a

Packaged vegetables 47/48 72/77 34/41 10/10 163/176 92.6a
Cooked ham 25/25 7/12 3/9 3/10 38/56 67.9b
Yogurt 71/100 27/75 51/64 6/31 155/270 57.4b
Mayonnaise bases deli-salads 47/50 24/76 7/23 0/14 78/163 47.9bc
^te
Pa  12/17 1/14 3/5 2/2 18/38 47.4bcd
Fermented meat sausages 6/8 7/12 8/17 0/12 21/49 42.9bcd
Other meat products 12/17 6/26 6/10 0/11 24/64 37.5bcd
Cooked sausages 14/18 4/33 3/6 0/8 21/65 32.3cd
Other smoked and/or dried meat products 19/31 2/41 10/29 1/15 32/116 27.6cd
Soft cheeses 52/101 2/67 13/58 2/44 69/270 25.6d
Hard cheeses 8/31 1/55 1/64 3/31 13/181 7.2e

Total 331/464 156/491 144/331 30/191 661/1477

% 71.3 31.7 43.4 15.6 44.7

considerable sales and consumption in Belgium and for which non-
respect of recommendations on shelf life and storage conditions
thus can have significant impact both with regard to food waste and
public health. The latter is illustrated by a number of outbreaks of
listeriosis linked to cooked meat products (Goulet et al., 1998;
Ha€chler et al., 2013; Mead et al., 2006). Thus, after having final-
ized the survey in the four supermarkets and being able to achieve
voluntary collaboration with a cooked meat production unit for this
challenge testing study, a pre-packed cooked pork sausage product
marketed in supermarket 3 under a private label, carrying a ‘best
before’ label, a recommendation of storage at < 7  C and an expiry
date set at 13 days after production was taken as a case study to
evaluate the validity of the shelf life label under various tempera-
ture conditions for storage (often recommended storage tempera-
tures of 4  C and 7  C and 10  C as an example of temperature
abuse). The challenge test was performed according to a protocol
that is based upon the EU Community Reference Lab (EU CRL)
guidelines for challenge testing (AFSSA, 2008) and that was pre-
viously executed in our lab as described by Uyttendaele et al. (2004)
and Vermeulen, Devlieghere, De Loy-Hendrickx, and Uyttendaele
(2011). In short, three L. monocytogenes strains, i.e. LMG 23192
^te
isolated from liver pa , LMG 23194 isolated from hard cheese and
LMG 26484 isolated from tuna-deli-salad, were cultivated sepa-
rately in 10 mL Brain Heart Infusion (BHI) broth (Oxoid) from glass
beads in the cryo-stock for 24 h at 37  C. A subculture of 0.1 mL was
made in 10 mL Brain Heart Infusion (BHI) broth (Oxoid) and incu-
bated for 24 h at 37  C. All subcultures were then individually
subjected to cold adaptation, namely incubation at 7  C for 4 days.
The inoculum for the challenge tests consisted of an equal volume
mix of these three L. monocytogenes cultures, of which the exact
concentration was determined by plating of the appropriate di-
lutions in Peptone Physiological Salt solution (PPS, consisting of
1.0 g/L Neutralised Bacteriological Peptone (Oxoid) and 8.5 g/L NaCl
(SigmaeAldrich)) on Tryptone Soya Agar Yeast Extract (TSAYE,
containing 40 g/L Tryptone Soya Agar (Oxoid) and 5 g/L Yeast
Extract (Oxoid)) and Agar Listeria Ottaviani Agosti (ALOA, Biolife).
Individual packages of the sliced pork sausage meat (200 g per
package) were obtained from the production unit providing su-
permarket 3 with this private label cooked meat product. Packages
were obtained 1 day after actual production and were prior pre-
served and transported to the lab under refrigerated conditions
(<4  C). Upon arrival in the lab, one package was subjected to
presence/absence testing for L. monocytogenes (per 25 g) using the
VIDAS® L. monocytogenes II method (Biome rieux) performed ac-
cording to the manufacturer's instructions to ensure that no natural
contamination was present. In parallel, samples of 225 g portions of
sliced cooked pork sausage meat were taken from the packages
obtained from the production unit, put in sterile black plastic trays
(Decatrays®, Decapac), inoculated with 225 mL of the mixed strain
inoculum (2000-fold and 40,000-fold diluted in PSS to obtain
inoculum levels of approx. 1000 and 50 CFU per g of cooked meat
product) and re-packed under modified atmosphere (30% CO2 and
70% N2) by sealing the tray with a top foil (Opalen HB 65 AF PP PL,
Bemis Packaging Benelux) using the Meca 900 (Decatechnic)
traysealer. After inoculation and packaging, three packages were
taken to determine the thus obtained initial inoculum level for
L. monocytogenes by enumeration. The remaining inoculated
packed cooked meat products (three packages per storage condi-
tion) were next stored in a temperature controlled refrigerator at
4  C, 7  C or 10  C. At the end of shelf life (13 days), three packages
of the cold-stored cooked pork sausage meat product were
analyzed for the total (psychrotropic) count, lactic acid bacteria and
L. monocytogenes by plating on respectively Plate Count Agar (PCA,
Oxoid), acidified (pH 5.7, obtained by addition of 8 mL 37% HCl
(SigmaeAldrich) prior to autoclaving) Man Rogosa Sharpe Agar
(MRS, Oxoid) and ALOA (Fiers). A sample of approx. 30 g was taken
from one package, tenfold diluted in PPS and homogenized in a
stomacher bag for 1 min (Colworth Stomacher 400, Lame ris). One
mL of the appropriate tenfold dilutions in PPS was added to PCA
pour plates and incubated at 22  C for 4e5 days, 1 mL was added to
acidified MRS pour plates with a secondary top layer to ensure
micro-aerophilic conditions during the incubation at 22  C for 4e5
days and 0.1 mL was put on ALOA spread plates and incubated at
37  C for 2 days.
3. Results
3.1. Shelf life labels and storage instructions on refrigerated food
products in supermarkets
In total 1477 refrigerated food items on display at the time of
visiting the four different supermarkets in Belgium were studied
with regard to their labeling of shelf life and storage instructions. It
was noted, as expected, that there is variation in the labeling ac-
cording to the food product category under consideration.
Furthermore, it was revealed that both within a defined food
product category as well as among different supermarket chains
there was quite some variation in the allocation of the type of shelf
life label (‘use by’ or ‘best before’ date) (Table 1) and the storage
temperature instructions (Table 2). Fifteen products were excluded
380 S. Ceuppens et al. / Food Control 59 (2016) 377e385

Table 2
The prevalence of storage conditions on refrigerated food products per supermarket and shelf life indication after opening of the package.

Storage and shelf life information Supermarket 1 Supermarket 2 Supermarket 3 Supermarket 4 Total

Storage temperature
None 31/464 20/491 29/331 3/191 83/1477 5.7%
Store cool 16/464 0/491 22/331 2/191 40/1477 2.7%
Max. þ4  C 165/464 14/491 43/331 3/191 226/1477 15.2%
Max. þ5  C 1/464 0/491 3/331 0/191 4/1477 0.3%
Max. þ6  C 55/464 29/491 42/331 9/191 135/1477 9.1%
Max. þ7  C 186/464 411/491 172/331 165/191 916/1477 62.0%
Max. þ8  C 26/464 14/491 18/331 9/191 67/1477 4.5%
Max. þ10  C 2/464 2/491 1/331 0/191 5/1477 0.3%
Max. þ12  C 0/464 1/491 0/331 0/191 1/1477 0.1%
Max. þ16  C 0/464 0/491 1/331 0/191 1/1477 0.1%
Shelf life after opening
No information 405/464 360/491 245/331 171/191 1182/1477 80.0%
Limited shelf life 11/464 116/491 20/331 6/191 154/1477 10.4%
Consume shortly after opening 5/464 6/491 5/331 2/191 18/1477 1.2%
A few days 0/464 6/491 3/331 2/191 10/1477 0.7%
1 day 6/464 0/491 7/331 0/191 13/1477 0.9%
1e3 days 4/464 0/491 0/331 0/191 4/1477 0.3%
2 days 10/464 0/491 26/331 0/191 35/1477 2.4%
2e3 days 5/464 0/491 0/331 0/191 4/1477 0.3%
3 days 12/464 0/491 13/331 6/191 31/1477 2.1%
3e4 days 0/464 0/491 1/331 0/191 1/1477 0.1%
4 days 0/464 0/491 2/331 0/191 1/1477 0.1%
5 days 1/464 2/491 1/331 3/191 7/1477 0.5%
1 week 5/464 1/491 5/331 0/191 12/1477 0.8%
2 weeks 0/464 0/491 3/331 1/191 4/1477 0.3%

from further analysis: (i) because there was no shelf life label
present on the product (n ¼ 5, mainly vegetables) or (ii) both ‘use
by’ and ‘best before’ labels were present (n ¼ 6, mainly yogurts), or
(iii) the presence of conflicting information e.g. a ‘best before’ label
with the instruction to consume the product at the set expiry date
at the latest (n ¼ 2) and (iv) the presence of an incorrect and unclear
shelf life label e.g. ‘use best before’ (n ¼ 2). The highest consistency
in the allocation of the shelf life label was observed with smoked
salmon (100% of products with ‘use by’ label, n ¼ 29) and pre-
packed (fresh-cut) vegetables (93% of products with ‘use by label’,
n ¼ 176), while hard cheeses were mostly carrying a ‘best before’
label (93%, n ¼ 181). Other food product categories comprised a mix
of both shelf life labels, ranging a proportion of 26% of soft cheeses
with a ‘use by’ label to 68% of ‘use by’ label for cooked ham. Su-
permarket 1 and 3 were supermarket chains from Belgian origin,
whereas supermarket 2 and 4 belonged to supermarket chains with
headquarters in a neighboring European country. The Belgian su-
permarket chains showed a significantly increased use of ‘use by’
labels (60% of all products, n ¼ 795) in comparison with the non-
Belgian supermarket chains (27%, n ¼ 682) (p < 0.001). This dif-
ference was statistically significant in all food products categories,
except for smoked salmon, pre-packed vegetables, fermented meat
sausages and hard cheeses.
A considerable proportion of the refrigerated food products in
supermarkets did not carry any (5.7%, 83/1477) or unspecific (2.7%,
40/1477) recommendations about storage conditions on the pack-
age (Table 2). The overall predominant recommendation was to
store the product at a temperature of maximum 7  C (62%, 916/
1477). The second most frequent recommendation was to store
food products at 4  C (15%, 226/1477), the latter originating mainly
from food products at supermarket 1, in which this type of storage
conditions was more noted (36%) than in supermarket 2, 3 and 4
(2.9%, 13% and 1.6%, respectively). In the case of smoked salmon, for
all individual food items displayed in all supermarkets at the time
of the visits the same storage condition, namely store at maximum
4  C was noted (Table 3). More variability was observed in the
labeled storage conditions for food products from other categories.
Supermarket 4 showed the highest uniformity in
recommendations in storage conditions: in 9 out of 12 food cate-
gories all products carried a label mentioning to store at maximum
7  C. Furthermore, it was observed that the majority of the refrig-
erated food products gives the consumer no indication of the
remaining shelf life after opening of the package (80%, 1182/1477)
or a vague description such as ‘limited shelf life’ or ‘consume
shortly after opening’ (12%, 172/1477) which is open to subjective
interpretation by the consumer (Table 2).
3.2. Stakeholder opinions on shelf life labels
Feedback on the survey results described above was collected
from the quality managers of the four visited supermarket chains as
well as the quality managers of four selected cooked meat pro-
duction companies in Belgium and a representative of the Belgian
Federal Public Service of the Public Health, Food Chain Safety and
Environment (FPS PHFSE). When asked whether they were aware
of the mixed use of 'use by' and 'best before' labels for different food
items within one food category and whether they would prefer to
get agreements on the use of one defined shelf life label per defined
food category in all supermarkets in Belgium, the following re-
flections were made. All retailers and the FPS PHFSE indeed knew
about the differences in shelf labels occurring and mentioned that it
would be challenging to get more uniformity in setting the labels.
As the product formulation and packaging atmosphere as well as
the initial microbial contamination level may differ amongst indi-
vidual food manufacturers, food items within a food product
category may or may not support or inhibit the growth of micro-
organisms (pathogens or spoilage organism) to a different extent
and thus variation in shelf life label, even within a food product
category is to be expected. One retailer highlighted that there
should be flexibility in assigning a shelf life label as there might be
innovative production/preservation methods which might indeed
enable to ensure safety and quality throughout a prolonged shelf
life (e.g. enabling also to have a ‘best before’ label for usually
assumed perishable products). It was a common reply among all
those consulted that it is the producer's responsibility to allocate
the shelf life label and set the expiry date. Still one supermarket
 S. Ceuppens et al. / Food Control 59 (2016) 377e385 381

Table 3
The predominant storage condition per food category and per supermarket with its prevalence (%) on the retail items.

Food product category Supermarket 1 Supermarket 2 Supermarket 3 Supermarket 4 Total


Smoked salmon Max. þ4 C Max. þ4  C Max. þ4 
C Max. þ4 
C Max. þ4 
C
100.0% 100.0% 100.0% 100.0% 100.0%

Hard cheeses Max. þ7 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
61.3% 85.5% 92.2% 90.3% 84.5%

Packaged vegetables Max. þ7 C Max. þ7  C Max. þ4 
C Max. þ7 
C Max. þ7 
C
79.2% 100.0% 58.5% 100.0% 71.6%

Other smoked and/or dried meat products Max. þ4 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
80.6% 97.6% 82.8% 100.0% 70.7%

Mayonnaise based deli-salads Max. þ4 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
80.0% 100.0% 69.6% 100.0% 68.7%

Fermented meat sausages Max. þ4 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
100.0% 50.0% 76.5% 100.0% 63.3%

Cooked sausages Max. þ4 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
94.4% 90.9% 50.0% 100.0% 63.1%

Other meat products Max. þ4 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
82.4% 84.6% 40.0% 100.0% 59.4%

Cooked ham Max. þ4 C Max. þ4  C/þ7  C Max. þ7 
C Max. þ7 
C Max. þ4 
C
96.0% 41.7%/41.7% 55.6% 100.0% 57.1%

Yogurt Max. þ7 C Max. þ7  C Max. þ6 
C Max. þ7 
C Max. þ7 
C
50.0% 64.0% 56.3% 83.9% 56.3%

Soft cheeses Max. þ7 C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ7 
C
49.5% 70.1% 27.6% 65.9% 52.6%
^te
Pa  Max. þ4 
C Max. þ7  C Max. þ7 
C Max. þ7 
C Max. þ4 
C
100.0% 92.9% 60.0% 100.0% 50.0%

mentioned that per food category they had internal assumptions on
whether it would be a ‘use by’ or a ‘best before’ label and if the
producers' suggestion of shelf life label deviates from it they would
inquire further information. Still this dialog on shelf life label may
only happen for the food items which are manufactured under the
retailers' private label. For (inter)national (premium) brands the
setting of the shelf life label is entirely the producers' responsibility
and is accepted without further dialog. FPS PHFSE confirmed that if
further agreement on a defined label per food category would be
needed, this should be tackled at EU level as indeed, as was the case
in the survey, retailers are based in one EU country but also have
supermarkets in neighboring countries which all are centrally co-
ordinated from one headquarter office. Also international (pre-
mium) brands setting a shelf label usually do not set different labels
for the same food item in different supermarkets in different
countries in EU. Still one supermarket did mention that the
guidelines on how to determine a shelf label are quite vague and a
clearer guidance would be welcome. The latter was also confirmed
by the majority of the quality managers of the cooked meat product
manufacturers that were consulted. The latter were only dealing
with one defined food category and 2 out of 4 were not aware about
the use of different shelf life labels for this cooked meat product
category. One mentioned that per definition, for this type of
product he assumed a ‘use by’ label. Three out of four indeed would
prefer to have more clarification on the setting of shelf life labels.
One suggested it would be clearer if indeed all products with a
(limited) shelf life of x days would automatically be allocated a ‘use
by’ date (x could be agreed upon by the sector organization, pref-
erably in accordance with the retailers and FPS PHFSE). One pro-
ducer also mentioned that safety aspects for the consumer should
be dominating in setting the shelf life label. The most precautionary
approach for cooked meat products would be setting a ‘use by’ date
and setting the expiry date assuming storage at 7  C. In contrast, the
same producer suggested that some fermented or dried meat
products may be quite stable and thus be allocated a ‘best before’
data rather than a ‘use by’ date as was noted in the survey.
As for the storage temperature recommended on the package,
FPS PHFSE mentioned the obligation to respect the legal maximum
temperature i.e. 4  C for fresh meat (not taken up in the present
survey), minced meat, meat preparations and fresh fish and fish-
eries products (including smoked salmon taken up in the present
survey) whereas all other (pre-packed) microbiological unstable
food products need to be kept at or below a maximum 7  C (Belgian
Royal Decree, 2014). Supermarkets generally follow (and assume
their suppliers to follow) the legal obligation on storage tempera-
ture. Again, the indication of storage conditions on the package is
the producers' responsibility. One producer mentions that overall
to ensure safety and quality of the product 4  C is preferred to 7  C,
as 4  C may slow down microbial growth and enhance the shelf life
duration. One producer mentions that retailers prefer a prolonged
shelf life (and mention this is important factor, often demanded by
retailers for private labeled manufactured meat products) as this
fits better in the retailers' logistic planning and provides them
multiple days for display of the food item in the refrigeration cab-
inets while providing also consumers at the time of purchase still
some remaining shelf life. However, if recommending storage at
4  C this should also be respected in retail and preferably also at
consumer (refrigerated) storage which is out of control of the
producers. For this reason, the producers mention that still often a
recommended storage temperature of 7  C is labeled. It is
acknowledged by the majority of producers and SPF PHFSE that
agreement of one storage temperature would be preferred, but the
majority of retailers seem to be doubtful whether this can be ach-
ieved currently.
On the question if they were aware that most food products
provide no information about the remaining shelf life after opening
of the package, the consulted producers and retailers replied they
have no grip on consumer behavior once the package is opened and
thus less likely to have recommendations on this. The SPF PHFSE
acknowledges that this type of information would be useful for the
consumer and there is a general communication of the Belgian
competent authorities to the consumer to keep opened packages of
perishable foods for max. 48 h in refrigerator (at temperature be-
tween 1 and 5  C).
Finally on the concluding question on whether they agree on the
criticism that shelf life labels contribute to food waste there was a
mixed reaction. Half (2 out 4) of the producers and half (2 out of 4)
of the retailers as well as the SPF PHFSE agreed on this, but still the
382 S. Ceuppens et al. / Food Control 59 (2016) 377e385
majority made reflections that one will need to have a shelf life
label. For sure, for communicating potential food safety issues of
expired perishable food products the ‘use by’ label is highly
important, but also consumers have the right to be informed on
(guaranteed) acceptable quality and should also be warned on
potential off-odours or off-flavors, deviating texture or rancidity
etc. occurring when products have passed the ‘best before’ date.
Main remark was that there is indeed the need to raise awareness
with consumers about the different meaning of the two shelf labels
i.e. ‘use by’ versus ‘best before’ and thus it being important in this
context to explain better to consumers the difference between
spoilage and safety.
3.3. Challenge test with L. monocytogenes to evaluate the shelf life
label of a pre-packed sliced cooked pork sausage meat product
Cooked pork sausage meat products of different independent
(premium) brands and the supermarket's own private label brands
were offered for sale in all supermarkets that were visited. For many
of these food items, different types of shelf life labels were used.
Supermarket 1 had six different cooked pork sausage meat products
in the refrigeration cabinet which all carried a ‘use by’ date and
recommended storage at maximum 4  C. These six food items
included whole sausages from three independent brands A, B and C
and from two own private label brands D and E (whole sausages and
pre-cut slices). Cooked pork sausage meat product of independent
brand C was also offered in supermarket 3 (also with a ‘use by’ label
and storage at max. 4  C), in addition to cooked pork sausage meat
product from its own private label brand F, the latter carrying a ‘best
before’ label and recommended storage temperature of max. 7  C.
Supermarket 2 had only one cooked pork sausage meat product
from its own private label brand G, with a ‘best before’ date and
storage at max. 7  C. Supermarket 4 sold two different cooked pork
sausages from own private label brand H and I and both carrying a
‘best before’ label and a max. 7  C storage recommendation. To
evaluate the validity of the set shelf life label and expiry date, as an
example, the pre-packed sliced cooked pork sausage meat product
of the private label brand F from supermarket 3 was selected for a
challenge test with a cocktail of three L. monocytogenes strains
inoculated at approx. 50 and 1000 CFU/g in triplicate and stored at
often recommended temperatures 4  C and 7  C and at 10  C as
representative for storage at temperature abuse. L. monocytogenes
showed >0.5 log CFU/g outgrowth at the end of shelf life (13 days) at
all tested storage temperatures, namely respectively outgrowth for
the 2 inoculum levels was established at 4  C: þ1.3 and 0.9 log CFU/
g; at 7  C: þ2.5 and 2.3 log CFU/g; and at 10  C: þ4.8 and 3.2 log CFU/
g (Fig. 1). The substantial multiplication of L. monocytogenes in-
dicates that if a (low) initial contamination level of ca. 5 CFU/g would
be present, within 13 days at 4  C it might reach levels of ca. 100 CFU/
g, the threshold level for recall of ready-to-eat foods from the market
(EC, 2005). It should be mentioned that the actual shelf life period
was even longer than 13 days as the 13 days was the remaining shelf
life of the investigated package taken in the supermarket. Growth of
L. monocytogenes during the entire shelf life period could therefore
even be higher than the one observed in the 13 days of remaining
shelf life in the present experiment.
If L. monocytogenes would be present at ca 1 CFU per 10 g,
storage at 7  C (as was recommended for this food item) the
pathogens' numbers at the expiry date could also be expected to be
near this threshold level 100 cfu/g, or exceed it in case of temper-
ature abuse (10  C) and thus not complying to the food safety
criteria for L. monocytogenes in ready-to-eat foods on the market as
stated in current EU legislation (EC, 2005). This indicates that a ‘use
by’ date would be more appropriate in this case study than a ‘best
before’ label and also the manufacturer would need to ensure good
manufacturing practices in order to achieve absence of
L. monocytogenes per 25 g in a multi-sample plan (usually n ¼ 5
according to EC, 2005). From the challenge test results it was noted
that the indigenous lactic acid bacteria also showed significant
outgrowth after 13 days storage although they could not inhibit the
growth of (artificially inoculated) L. monocytogenes. The lactic acid
bacteria dominated the microbiota on the cooked meat product but
at the expiry data numbers present were (just) below the 7.0 log
CFU/g (at 4  C and 7  C) and thus near but not exceeding the
threshold level for causing adverse sensorial properties of the
product (Lahou, Jacxsens, Daelman, Van Landeghem, &
Uyttendaele, 2012). As such the expiry data was appropriately set
with respect to the spoilage organisms and did not lead to a dete-
riorated product throughout the recommended shelf life.
4. Discussion
Our former study indicated that less than half of the Belgian
consumers fully understand shelf life labels (Van Boxstael et al.,
2014). According to the technical report on food waste across EU
27 (EC, 2010), the current food labels, i.e. ‘best before’ and ‘use by’,
should be clarified and standardized to increase the consumers'
knowledge and awareness of food edibility criteria and reduce food
waste originating from date label confusion. For a few product
categories there seems to be a rather consistent application on the
type of shelf life label (e.g. smoked salmon always carried a ‘use by’
date and hard cheeses predominantly a ‘best before’ date). For other
products, in particular fermented products which are generally
recognized as safe foods, such as fermented meat sausages and
yogurt, the assignment of a ‘best before’ date would be expected. It
is not clear if there was a rationale for occasionally setting a ‘use by’
date. For other food categories such as known at risk products for
listeriosis i.e. soft cheeses and cooked meat products, there was also
a mixed use of shelf life label. For the mayonnaise based deli-salads
(sandwich spreads with egg, chicken, fish, ham, etc) which may
differ in pH or preservatives a mixed use of shelf life labels was
expected. For example, depending on the water activity, the pH and
the concentration of acetic acid, sorbic acid and benzoic acid in
mayonnaise-based deli-salads, L. monocytogenes may not be able to
grow in these deli-salads (Vermeulen et al., 2006) and thus might
be allocated a ‘best before’ date under these circumstances. Simi-
larly, based upon predictive modeling, no growth of
L. monocytogenes is expected to occur for example at 7  C for cooked
meat products when pH is 6.2, aw is 0.96 and a modified at-
mosphere of minimum 50% of CO2 is used in combination with
minimum 1.5% sodium lactate (Devlieghere et al., 2001). Indeed in
performing challenge testing of a range of commercially developed
cooked meat products and mayonnaise based deli-salads, it was
noted that for specific food products growth of L. monocytogenes
was not supported within the set duration of shelf life (at 4e7  C)
(Uyttendaele et al., 2009). Thus depending upon the exact combi-
nation of pH, aw, preservatives, packaging atmosphere and the
presence of competing microbiota the food product under consid-
eration may or may not allow the growth of L. monocytogenes
whereas these differences in composition of the product or the
packaging may not be noticeable to the consumer buying the
product on display in the supermarket. Thus, consumer confusion
about shelf life labels can be partially attributed to mixed occur-
rence of ‘use by’ and ‘best before’ dates within one food category,
which may persuade some consumers to treat the different shelf
life labels similarly. However, as mentioned above from a technical
point of view, due to variation in product formulation and pack-
aging atmosphere, a fraction of products within one food category
may indeed carry a ‘use by’ date while others have a ‘best before’
date. Thus, it is important to communicate to consumers better the
 S. Ceuppens et al. / Food Control 59 (2016) 377e385 383

Fig. 1. Cooked pork sausage inoculated with Listeria monocytogenes at low (approx. 50 CFU/g) and high (approx. 1000 CFU/g) concentrations and stored at 4  C, 7  C and 10  C until
the end of shelf life (13 days). Concentrations of L. monocytogenes, lactic acid bacteria and total bacterial count presented are the average of triplicate samples and error bars present
the standard deviation.

meaning of and the difference between ‘use by’ and ‘best before’
dates.
The Belgian federal food safety agency has issued a leaflet to
increase awareness on the use of these labels for consumers and
also issued some guidelines on the use of these labels to food
business operators in 2011. Also other competent authorities and
organizations have made guidelines available on setting of shelf life
labels (e.g. DEFRA, 2011; Food Safety Authority of Ireland, 2014;
New Zealand Food Safety Authority, 2005). Still in the present
consultation of stakeholders it was mentioned that guidelines are
quite vague and there seems to be a need for clarification. Usually,
in many refrigerated ready-to-eat foods with a prolonged shelf life,
L. monocytogenes growth potential is the limiting factor in ensuring
safety and determinative in assigning the shelf label and establish
the expiry date. To assess L. monocytogenes growth potential one
makes use of a combination of knowledge on product characteris-
tics, predictive modeling, challenge testing and durability studies
(annex II of Regulation 2073/2005). Still, the storage temperature
will have an impact on the outcome of these tests.
However, from the current survey it was noted that no or un-
specific storage temperature was mentioned on respectively 5.7%
and 2.7% of the products. In the Belgian context the label “keep
refrigerated” relates to the legal temperature maximum of 7  C. If a
specific temperature is mentioned, then it is often 7  C and occa-
sionally 4  C. In particular for smoked salmon there is unanimous
agreement on both assigning a ‘use by’ date and recommended
storage at 4  C (because of the legal obligation). To restrict the
growth of any pathogens, but in particular to inhibit the growth of
L. monocytogenes, temperature control throughout the distribution
and storage both at retail and at the consumers' home is required.
In the period January 2010 to January 2012 over 10,000 batches
of either packaged smoked or gravid fish, cooked meat products
and soft or semi-soft cheeses were sampled in supermarkets or
small shops in 26 EU Member States and Norway in order to esti-
mate the prevalence of L. monocytogenes in certain ready-to-eat
foods. On this occasion also samples' surface temperature at retail
was measured. There appeared to be some variation but surface
temperature recorded at retail in the vast majority of products was
7  C or below, few exceptions with a temperature at 10  C or above.
The mean storage temperature at retail was respectively 3.7  C with
standard deviation of 1.8  C for surveyed meat samples, 3.5  C with
a standard deviation of 1.8  C for surveyed fish samples and 4.1  C
with a standard deviation of 1.8  C for surveyed cheese (EFSA,
2013). Still, it could be questioned to which extent the recom-
mended 4  C or 7  C as storage temperature at the label can or will
also be ensured during remaining shelf life after purchase in the
consumers' refrigerator. Recently the Belgian Federal Safety Agency
issued recommendations to consumers to keep refrigerators at
1e5  C. The majority of Belgian households does not comply with
the recommended storage conditions on refrigerated food
384 S. Ceuppens et al. / Food Control 59 (2016) 377e385
products. The average temperature of the fridge of Belgian house-
holds is 6.7  C, only 27% of the domestic refrigerators was set at
optimal temperatures (5  C) and as much as 46% were determined
to have a temperature of more than 7  C of which 11% was even at
temperatures 10  C (n ¼ 3001) (Devriese, Huybrechts, Moreau, &
Van Oyen, 2004). The results of this Belgian study are in line with
other European studies on domestic cold-storage temperatures
(EFSA, 2007). In the UK, approximately 80% of consumers know the
correct temperature for their refrigerator, but only 20% actually
measured the temperature and the majority ‘feels’ the food to make
sure it is cold enough (Lyndhurst, 2011). And even if the thermostat
of domestic refrigerators was set at the maximum level of cooling,
36.1% (13/36) offered insufficient cooling capacity, i.e. the temper-
atures were 5  C (Flynn, Blair, & McDowe, 1992).
The shelf life period of a specific food product is defined by the
manufacturer who takes into account food safety parameters (food
safety risk) and/or quality parameters (microbial, chemical and
physical spoilage potential) as limiting factors (Van Boxstael et al.,
2014). It is up to the manufacturer to decide at which tempera-
ture he will execute the challenge test and some variation in tem-
peratures used was being observed, also depending upon the type
of food category, but most of the time challenge testing occurred at
4e5 or 7e8  C or a combination thereof (Uyttendaele et al., 2009).
The EU-Reference Lab guideline for challenge testing of
L. monocytogenes (EU-RL, 2014) states a quite high temperature
(12  C) at retail and consumer storage, but mentions that any other
temperature justified by detailed information i.e. the 75th
percentile of the observations for the country where the stage of
the cold chain is located. Overall, the temperature of a shelf life test
can be either 4e5  C e in particular if the manufacturer judges to
have an appropriate product formulation and packaging in order to
be able to slow down growth and along with a low storage tem-
perature seeks to prolong the shelf life which, as one manufacturer
mentioned in the present study, is often preferred by retailers for
logistic reasons. Or, more often, the storage temperature used in
setting the shelf life is 7  C. This is the Belgian maximum legal
temperature to keep microbiologically unstable food products and
was recently also mentioned as acceptable temperature in the
guideline of the Belgian food safety authority for L. monocytogenes
challenge testing as 7  C is indeed a temperature representative for
the Belgian consumers' home refrigerator. However, if one seeks to
take into account potential temperature abuse that might occa-
sionally occur during consumers' storage, one may execute a
challenge test at 10  C Only exceptionally was 10  C noted as abuse
temperature in retail (EFSA, 2013) and usually 90% of consumers'
refrigerators in Europe are at or below 10  C (EFSA, 2007).
Still, if a shelf life label and duration was allocated based on test
executed at 4e5  C or 7e8  C, the expiry date may in reality be
ealier than the one indicated on the package due to temperature
abuse during storage of refrigerated products either at retail or by
the consumer. To illustrate what is effect of temperature on the
growth potential of L. monocytogenes, the validity of the set shelf
life duration and label of a cooked pork sausage meat product was
tested at 4, 7  C and 10  C. The set expiry date corresponded more
or less correctly with the time that spoilage could be expected due
to outgrowth of naturally present lactic acid bacteria (107 cfu/g).
But this also showed that the cooked meat products may still
appear acceptable without sensorial deviations to be noticed while
containing hazardous levels of L. monocytogenes. Thus the food
producer seemingly assigned incorrectly a ‘best before’ label as
L. monocytogenes could, if accidentally present, multiply to
numbers exceeding the threshold level of 100 CFU/g during the
shelf life duration under the recommended (7  C) storage condi-
tions. Also Glass and Doyle (1989) observed refrigerated vacuum
packaged cooked ham to be still organoleptically acceptable when
it contained >100 CFU/g of L. monocytogenes. Cooked meat products
are known to be occasionally contaminated with L. monocytogenes
(EFSA, 2007; Gilbert et al., 1993). In meat products, the EU preva-
lence of L. monocytogenes-contaminated samples at the end of
shelf-life was 2.1% (n ¼ 3530) while the EU-level of samples
exceeding the level of 100 CFU/g was 0.4% and with higher odds of
L. monocytogenes presence for sliced samples compared to non-
sliced samples. In the period 2005e2007, during analysis of
various cooked meat products set for sale on the Belgian retail
market, a prevalence for L. monocytogenes of 1.1% (7/639) was
noted, with none of the samples exceeding 100 CFU/g (Uyttendaele
et al., 2009). In the latter study, also challenge testing was per-
formed on multiple cooked meat products kept during the actual
shelf life at 4  C or 7  C or a variable temperature schedule of e.g.1/3
of shelf-life at 4  C and 2/3 of shelf-life at 7e8  C as defined by food
business operator, which showed growth potential of (artificially
inoculated) L. monocytogenes in the majority (66.3%, 61/92) of
cooked meat products. It is known that cooked meat products allow
the outgrowth of L. monocytogenes when stored at refrigeration
temperatures unless modified atmosphere packaging (with
increased CO2 level) in combination with lactate and/or acetate is
used as a preservative. Given the FAO/WHO Listeria risk assessment
(FAO/WHO, 2004) it was concluded that most listeriosis cases are
due to ready-to-foods being contaminated at the time of con-
sumption with numbers of L. monocytogenes above the limit of
100 cfu/g with e as also stated by a follow-up EFSA opinion (EFSA,
2007) e most listeriosis cases in risk assessment studies estimated
to be due to foods with pathogen contamination markedly above
the latter limit. This was the basis of the current EU legislation (EC,
2005) stating food safety criteria to verify that no single sample of a
ready-to-eat food product exceeds the level of 100 cfu/g at the end
of shelf life (being the expected ultimate date of consumption for
ready-to-eat foods with a “use by” shelf life label), if a multiple
sample subunit approach (n ¼ 5) has been followed. However, the
actual impact on public health for a sample exceeding the limit of
100 cfu/g would depend to which extent the level of
L. monocytogenes contamination is markedly above this threshold
value, and also the susceptibility of the human host ingesting the
food, and the amount of food being eaten. Thus, indeed ready-to-
eat food samples potentially exceeding the limit of 100 cfu/g at
the end of the set shelf life are not complying to EU legislation (EC,
2005) but the impact on public health is uncertain.
Taking the above into account as well as the feedback collected
by the stakeholders, it seems that there is a need for clearer
guidelines on setting of the shelf life label. Overall it would be
useful to allocate to one food category one type of shelf life label,
which would ensure clarity to the producer/retailer and avoid
confusion with consumers on how to handle these food products.
However, as mentioned above there are arguments pro and con of
allocating one uniform shelf life label to one food category. In
addition, as already noted in the present survey in shops of four
different supermarket chains, harmonization is a difficult issue, not
only within a country but for sure also between different countries
as many food products are traded across borders and supermarket
chains may have subsidiaries in many countries.
5. Conclusion
Shelf life labels are intended to inform consumers on how to
handle pre-packed food products. Former studies (Van Boxstael
et al., 2014) revealed that the Belgian consumer has a poor un-
derstanding of the meaning of the two types of shelf life labels as
stipulated by the European legislation. The current study shows
that producers of refrigerated products in Belgium use different
types of shelf life labels for the same type of products. The type of
 S. Ceuppens et al. / Food Control 59 (2016) 377e385
label on a specific food category also seems to vary depending upon
the supermarket chain when selling these products under private
label. Moreover, the storage instructions on the package are vari-
able. It is clear that this mixed use of shelf life labels and storage
recommendations may further confuse the consumer on how to
handle food. Both with respect to food waste and food safety, more
attention is needed to reflect, as an individual company or an in-
dustry association or competent authority on more stringent
guidelines on the use and the validation of shelf life labels. To clarify
this situation, one might consider the following approaches (1)
either a fixed type of shelf life label is allocated at EU level to
specific food categories or even more simple (2) all refrigerated
food products are labeled with a ‘use by’ date and all non-
refrigerated food products are labeled with a ‘best before’ label.
The latter is the most simple method but will lead to more food
waste than the first option and a balance between contributing to
food waste versus ensuring maximum food safety will need to be
considered when setting shelf life labels.
Acknowledgments
This research was conducted in the framework of a Master
thesis in Bio-Science Engineering at Ghent Univeristy and also
supported by the Veg-i-Trade project (Grant agreement n .:
244994), which is funded under the Seventh Framework Pro-
gramme for Research of the European Commission. In addition, we
would like to thank the retailers and respondents involved in data
collection.
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