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Effectiveness of two sanitation procedures for


decreasing the microbial contamination levels
(including Listeria monocytogenes) on food
contact and non-food contact surfaces in a d...

Article in Food Control · January 2012


DOI: 10.1016/j.foodcont.2011.05.017

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Food Control 23 (2012) 26e31

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

Effectiveness of two sanitation procedures for decreasing the microbial


contamination levels (including Listeria monocytogenes) on food contact and
non-food contact surfaces in a dessert-processing factory
Montserrat Campdepadrós a, *, Alberto Miguel Stchigel a, Marta Romeu b, Joan Quilez c, d, Rosa Solà e
a
Microbiology Unit e Department of Basic Medical Sciences, Faculty of Medicine and Health Sciences, IISPV, Universitat Rovira i Virgili, C/ Sant Llorenç 21, 43201 Reus, Spain
b
Pharmacology Unit e Department of Basic Medical Sciences, Faculty of Medicine and Health Sciences, Universitat Rovira i Virgili, C/ Sant Llorenç 21, 43201 Reus, Spain
c
Human Nutrition Unit e Department of Biochemistry and Biotechnology, Faculty of Medicine and Health Sciences, IISPV, Universitat Rovira i Virgili, C/ Sant Llorenç 21,
43201 Reus, Spain
d
CIBER Fisiopatologia de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, Spain
e
Lipids and Arteriosclerosis Research Unit (CIBERDEM), Hospital Universitari Sant Joan, Faculty of Medicine and Health Sciences, IISPV, Universitat Rovira i Virgili, C/ Sant Llorenç 21,
43201 Reus, Spain

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

Article history: The aim of this study was to determine the presence and persistence of Listeria monocytogenes (LM) after
Received 21 December 2010 using two sanitization protocols in different parts of a dessert-processing factory. The sampling for LM
Received in revised form detection was performed: a) on various food contact and non-food surfaces; b) after and before treat-
19 May 2011
ment using two different sanitization protocols. LM was not detected on food contact surfaces while its
Accepted 24 May 2011
identification was restricted to non-food contact surfaces (mostly the floor). Both sanitizing protocols
managed to reduce the LM load (as well for the rest of the microbial parameter studied) but not to
Keywords:
eradicate the microorganism completely.
Contamination
Environments
Ó 2011 Elsevier Ltd. All rights reserved.
Food processing
Hygiene
Pastry

1. Introduction eat industrial products consumed without cooking or reheating


(Dalton et al., 1997; Leite et al., 2006; Lyytikäinen et al., 2000;
Listeriosis due to Listeria monocytogenes (LM), a food-borne Miettinen et al., 1999; Rocourt, 1996).
disease-causing bacterium can produce infections in susceptible LM is quite resistant to the deleterious effects of freezing, drying,
human populations, such as immunodepressed people, infants and and heating, despite not forming endospores, and can grow
pregnant women (Garrido, Torroba, Garcia-Jalón & Vitas, 2008; between 0 and 45  C (Bell & Kyriakides, 2005), surviving for long
Klontz et al., 2008), causing septicaemia, meningitis, meningo- periods in refrigerated, frozen and dried foods, and shows a high
encephalitis, foetus abortion, and death (Mead et al., 1999; tolerance to acidic conditions and high salt concentrations (Lou &
Vázquez-Boland et al., 2001; CDC, 2010). However, there are Yousef, 1999). LM also survives in lubricants employed in the food
several reports of a non-invasive form of listeriosis, which causes industry, especially when the lubricants are contaminated with
gastroenteritis, affecting persons with no (or unknown) predis- organic material and water (Aarnisalo, Raaska, & Wirtanen, 2007).
posing factors (Aureli et al., 2000; Salamina et al., 1996), as an LM is particularly difficult to control, since it is ubiquitous and
outbreak of febrile gastroenteritis associated with corn contami- widespread in nature, and because it possesses physiological
nated by LM. A variety of foods have been found to be contaminated characteristics that allow it to grow under conditions that are
with LM (Inoue et al., 2000). This occurs most frequently with soft usually adverse for most human pathogenic bacteria. Due to its
cheeses, dairy products, pâtés, sausages, smoked fish, salads, infant ubiquity, LM can produce several problems in food-processing
cereals, cakes, cream, butter and, in general, refrigerated ready-to- factories (Lundén, 2004; Møretrø & Langsrud, 2004). LM was iso-
lated in 4.27% of samples from cakes collected at different hotels,
restaurants and pastry shops over a year (Uhitil, Jaksic, Petrak,
* Corresponding author. Tel.: þ34 654139196; fax: þ34 977 759378. Medic, & Gumhalter-Karolyi, 2004). The bacterium usually enters
E-mail address: montserrat.campdepadros@urv.cat (M. Campdepadrós). the food through raw materials, water and workers. However, LM

0956-7135/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2011.05.017
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M. Campdepadrós et al. / Food Control 23 (2012) 26e31 27

has also been isolated from a large variety of food-processing S.L., Barcelona, Spain), a system for dispensing a wide variety of
equipment (Tompkin, 2002), and can persist in these for a long automatically diluted sanitizers. The surfaces in contact with food
time (Miettinen, Björkroth, & Korkeala, 1999). were rinsed with clean water, and dried with single-use flannels.
Normally, the routine application of good sanitization practices Surfaces not in contact with food were not dried.
should be capable of killing LM, but we must bear in mind that if Complementarily, an AerobrumerÔ (José Collado, S.A., Barce-
contamination levels are high, or the sanitization procedures are lona, Spain) was the equipment employed for air disinfection by
inappropriate, the transient micro-organisms may be able to thermal fogging with biocide agents.
establish themselves, then multiply and become resident (Kumar & The protocols employed for surface sanitizing were as follows:
Anand, 1998; Gram, Bagge-Ravn, Ng, Gymoese & Vogel, 2007).
LM is capable of forming biofilms, a multi-cellular layer of Protocol A: Applied daily. Visible dust was removed by manual
adherent bacteria surrounded by a matrix of extra-cellular poly- scanning. The surface was rinsed with warm water (45e50  C) at
saccharides (Costerton, Lewandowski, Caldwell, Korber, & Lappin- low pressure. Easyfoam VF32Ô (diluted to 3e4%) was applied
Scott, 1995; Wirtanen & Mattila-Sandholm, 1992). The biofilms and left for 15e20 min followed by manual scrubbing, and
composed of a range of multiple microbial taxa can form on abundant rinsing with tap water. Suredis VT 01 LÔ (diluted to
a variety of materials used in packaging and equipment, such as 1e2%) was applied and left for 15e20 min. Finally, it was rinsed
stainless steel, TeflonÒ and other plastics for packaging, rubber, abundantly with tap water. Weekly air disinfection was per-
glass and others (Krysinski, Brown, & Marchisello, 1992; Midelet & formed after work (Saturday afternoon to Sunday morning) (see
Carpentier, 2002; Sofia, Charalambia, Efstathios, Antonia, & George- below).
John, 2009). Thus, biofilms are an important reservoir for micro- Protocol B: Once every three weeks. Visible dust was removed
organisms, and have not received enough attention within food by manual scanning. The surface was rinsed with warm water
processing areas (Mittelman, 1998; Araújo & Carballo, 2004; (45e50  C) at low pressure. Easyfoam VF32Ô (diluted to 3e4%)
Unnerstad et al., 1996), particularly due to the resistance of LM to was applied and left for 15e20 min followed by manual scrub-
sanitizing agents employed in food-processing environments bing, and abundant rinsing with tap water. Aciplusfoam VF59Ô
(Blackman & Frank, 1996; Kumar et al., 1998; Pan, Breidt, Jr., & (diluted to 3e4%) was applied and left for 15e20 min. It was
Kathariou, 2006). then scrubbed manually, and rinsed abundantly with tap water.
Apart from the program to eliminate microorganisms in Suredis VT 01 LÔ (diluted to 3e4%) was applied and left for
industrial environments, effective cleaning and sanitation steps 15e20 min. Finally, it was rinsed abundantly with tap water.
must both be included to prevent the development of biofilms and Weekly air disinfection was performed after work (Saturday
reduce the possibility of food contamination. afternoon to Sunday morning) (see below).
The aim of this study was to detect the presence and persistence
of LM using two sanitization protocols at different points in Aerial treatments were performed with the electro thermal and
a dessert-processing factory. The first objective of our work was to molecular fogger. This emits a totally dry spray, either disinfectant
identify possible environments as sources of contamination by LM or insecticide, whose particles are between 0.5 and 1 mm large, to
but subject to structural improvements. The second objective was the environment. It is a process where the air is used as a means of
to assess the effectiveness of a variety of products commonly used transmission for the biocide aerosol, which has an effect on both
as sanitizers in food industries, and their methodology of imple- horizontal and vertical surfaces.
mentation. The knowledge acquired during this research could help Air disinfection: Thermal fogging with F-66TM and Divosan
in establishing microbiological critical control points, and would 2080 TNÔ from AerobrumerÔ, was alternated between both
suggest changes to cleaning protocols, the design and location of disinfectants every two months. The recommended product
some equipment, and/or of work schedules in the factory. quantity for preventative treatment was 6 min misting every
100 m3 of establishment.
2. Material and methods
2.2. Sampling
2.1. Cleaning and sanitizer products
All surfaces analyzed were within the cake-making area. The
Two types of cleaning and disinfection agents were tested: food contact surfaces comprised all the elements and equipment on
Easyfoam VF32Ô (JohnsonDiversey España, S.L.) (2.71% sodium the production line made of stainless steel, rubber or plastic. Non-
hypochlorite, as active chloride; 7% sodium hydroxide; excipients, food contact surfaces included auxiliary elements, such as doors,
qs 100%) and Aciplusfoam VF59Ô (JohnsonDiversey España, S.L.) walls, floor, drains, and personnel access areas, made of stainless
(15e30% phosphoric acid; 5e15% nitric acid; excipients, qs 100%). steel, plastic, epoxy resins, aluminium or rubber. These surfaces
In both cases, Suredis VT 01 LÔ (JohnsonDiversey España, S.L.) (1.6% surround the food contact area, or are around the production lines.
N-(3-aminopropyl)-N-dodecylpropane-1,3-diamine; excipients, qs Before starting the sampling phase, and together with the
100%) was later applied to the treated surfaces. historical controls, a study was performed to identify those areas
Another hygienisation method was using alternatively F-66Ô with the highest levels of microorganisms. The microbial contam-
(José Collado S.A.) (0.25% benzalkonium chloride; excipients, qs ination parameters were analyzed: a) at the beginning of the
100%) and Divosan 2080 TNÔ (JohnsonDiversey España, S.L.) (3% workday; b) at the end of the workday, before sanitizing. These
glutaraldehyde; excipients, qs 100%) aerosolized. studies were conducted during 4 months in early 2009, sampling
The places where the sanitizers were applied included the the surfaces analysed three consecutive sequences of three times
pastry preparation, elaboration and packaging areas. The treat- with protocol A and once with protocol B. During this period,
ments were applied to cream dispensers, working tables, the factory produced several types of cakes with a variety of
conveyors, floors, drains, walls, doors, curtains, etc. The removable ingredients, and a wide range of raw materials and presentations.
parts of the equipment from the production lines were cleaned in The samples were obtained from two types of surface: food
the washing room. contact and non-food contact. The food contact surfaces included
The cleaning and disinfection agents were applied to the conveyor belts, equipment, dosage pipes, the freezing tunnel, and
surfaces with DivercleanÔ equipment (Johnson Diversey España, various tools. The second group consisted of floors, walls, cleaning
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28 M. Campdepadrós et al. / Food Control 23 (2012) 26e31

supplies, drains, a walk-through sole-washer system, and recircu- 2.4. Statistical analysis
lation air grilles. Surfaces suspected to be the sources of contami-
nation were investigated, as summarized in Table 1, which Pre-specified subgroup analyses were performed according to
describes the number of samples taken before and after cleaning, food contact and cleaning protocol during sampling (Table 1). The
according to the type of sanitizing protocol done. data were presented as means  SD. To test differences in groups,
The samples were obtained with pre-moistened sterile swabs. statistical significance was determined either by ANOVA and
The Path-Chek Hygiene Pathogen System from Microgen Bio- Student’s “t” tests for parametric data, or the KruskaleWallis and
products (Microgen Bioproducts Ltd., Camberley, UK) consisted of ManneWhitney U tests for non-parametric data. Two-sided p
two units; a pre-moistened Path-Chek Hygiene swab and Path- values of less than 0.05 were considered to indicate statistical
Chek Hygiene Detection Broths, a highly specific and sensitive significance. The data were analyzed with the use of SPSS statistical
detection media. The standard sample area of 10  10 cm was software, version 17.0.
evaluated. The swabs used for sampling were rubbed three times in
several directions. Samples were taken in duplicate. A sterile paper 3. Results
was used as a template to outline a selected area, inside which the
swabbing was done. If the sampled areas were irregular, or it was 3.1. Presence of LM before and after cleaning and sanitizing
not possible to take a standard sample, such as on the legs of tables
or machines, a sampling area of 100 cm2 was estimated de visu and A total of 285 analyses were carried out for TAPC and ENT, 323
processed as above. for M&Y, and 498 for LM. The presence of pathogenic bacteria
before and after sanitation of the production areas with both
2.3. Microbiological analysis protocols is shown in Table 2. Note that the presence of bacteria was
significantly higher in all cases in the samples taken before sani-
The following microbiological contamination parameters were tizing. The results indicate that the cleaning procedures were
evaluated for the selected surfaces to sample: total aerobic plate effective at reducing the presence of microorganisms, but unable
count (TAPC), Enterobacteriaceae (ENT), and mould and yeast to eliminate those completely. The values of TAPC and M&Y were
(M&Y) counts. TAPC, ENT and M&Y were determined by culturing low, even before sanitizing, with a mean of 4.9 (cfu/cm2) and 1.7
on plate count agar (PCA; Merck - España, Madrid, Spain), violet red (cfu/cm2) before cleaning and 2.8 (cfu/cm2) and 0.8 (cfu/cm2) after
bile glucose agar (VRBG; Oxoid España, S.A., Madrid, Spain) and cleaning, respectively. According to D 2001/471/EC, in the case of
chloramphenicol glucose yeast extract agar (CGY; Oxoid España, food contact surfaces, acceptable TAPC values are between 0 and
S.A., Madrid, Spain), respectively, and according to ISO 4833:2003, 10/cm2, and unacceptable if >10 cm2; for ENT, they are acceptable
ISO 5552:1997 and ISO 7954:1987. The results were given in colony between 0 and 1/cm2, and unacceptable > 1/cm2. The ENT average
forming units by surface area (cfu/cm2), in line with the microbi- before sanitizing indicates that the surfaces were initially “dirty”
ological criteria adopted in the D 2001/471/EC. (with a mean of 1.3 cfu/cm2), but acceptable (0.6 cfu/cm2) after
The Path-Check Hygiene Pathogen SystemÔ kit was employed cleaning. The LM showed a presence of 15.2% before cleaning,
for presumptive detection of LM. This detection system meets the falling to 6.9% after cleaning. There was a significant reduction in
requirements of ISO 18593:2004, but unlike similar methods, it the presence of LM after cleaning whichever sanitizing protocol
requires no pre-enrichment step. To obtain the samples, the cap was used (p ¼ 0.003). However, LM did not totally disappear and
from the pre-moistened Path-Chek Hygiene swab was removed, showed an ability to survive on floors that had undergone sani-
and it was swabbed on the surface of a pre-selected standard area, tizing treatments.
rotating it while performing this operation. The swab was then
placed in the tube of the Path-Chek Hygiene Detection Broth (if the 3.2. Presence of LM according to the type of sanitizing protocol used
swab could not be transferred immediately to the Path-Chek
Hygiene Detection Broth, it was returned to its holding tube and As mentioned above, clean-up operations reduced all microbial
stored at less than 20  C for not more than 24 h). The inoculated populations, including LM. Table 3 shows the results obtained
tubes, placed in a rack, were incubated for 24e48 h at 28e30  C. according to the type of sanitizing procedure (Protocol A or B)
Presumptive positive tests (turning from yellow to black) were employed. LM was detected in 15.2% of the places sampled before
confirmed by plating of a 0.1 ml of the Path-Chek Hygiene Detection sanitizing, 7% after applying protocol A and 5.9% after employing
Broth onto Chrom’ID Ottaviani Agosti agar (bioMérieux S.A., Marcy- protocol B. The decrease of the % of presence of LM was significant
l’Etoile, France), and incubating it at 37  1  C for 24e26 h. Blue after applying protocol A (p ¼ 0.007). Although there was a greater
colonies with halos were presumptive for LM and L. ivanovii. Five decrease in the percentage with protocol B, this cannot be
such presumptive colonies were grown on horse blood agar considered significant (p ¼ 0.05). This can be due to the small
37  1  C for 21e27 h, and the isolates were biochemically iden- sample size in the group of analyses carried out after cleaning with
tified by using APIÒ Listeria (bioMérieux S.A., Marcy-l’Etoile, protocol B (n ¼ 4).
France).
Table 2
Total aerobic plate count (TAPC), Enterobacteriaceae (ENT), moulds and yeasts
(M&Y), and Listeria monocytogenes (LM), before and after applying the sanitizing
Table 1
protocols.
Food contact and non-food contact surfaces sampled before and after sanitizing with
protocols A and B. Parameters measured Before cleaning After cleaning Significance

Before After After Total Mean  SD (n) Mean  SD (n) p


cleaning protocol A protocol B samples (%) TAPC (cfu/cm2) 4.9  5.3 (72) 2.8  4.3 (213) 0.006
Food contact 17 118 43 178 (36.6) ENT (cfu/cm2) 1.3  2.5 (72) 0.6  1.8 (213) 0.002
surfaces M&Y (cfu/cm2) 1.7  2.7 (84) 0.8  1.8 (239) 0.001
Non-food contact 147 137 25 309 (63.4) LM (% presence) 15.2 (164) 6.9 (334) 0.003
surfaces
Results are expressed as mean  Standard deviation (SD); n: number of samples; p:
Total samples (%) 164 (33.7) 255 (52.3) 68 (14.0) e
significance level between before and after cleaning.
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M. Campdepadrós et al. / Food Control 23 (2012) 26e31 29

Table 3 Table 5
Frequency and percentage of presence/absence of Listeria monocytogenes (LM) by Enumeration and description of the places where Listeria monocytogenes (LM) was
sanitizing protocol. detected.

Sanitizing Presence of LM, Absence of LM, Significance p Total Type of Locations in the Samples where Samples where
samples (%) samples (%) samples surfaces factory LM was absent LM was present
0 - Before cleaning 25 (15.2) 139 (84.8) e 164 Food contacting All places 178 e
1 - Protocol A 18 (7.0) 237 (92.2) 0e1 p ¼ 0.007 255 Non-food contacting Walls 9 e
2 - Protocol B 4 (5.9) 64 (94.1) 0e2 p ¼ 0.050 68 Doors 14 e
Air conditioning grid 7 e
Walk-through 17 5
sole-washer system
3.3. Relationship between TAPC, ENT, and M&Y counts and the Floor 127 41
presence/absence of LM Floor drains 5 e
Cleaning supplies 10 1 (sponge mop)

Table 4 shows the presence of selected microorganisms (TAPC,


ENT and M&Y) and their average, related to the presence/absence of
LM. The averages of all microbiological parameters studied were
places where these microorganisms, including LM, can survive and
higher in those cases where LM was detected, in comparison with
persist over time despite the sanitization treatment applied
those in which LM was not detected. The analyses indicated that the
(Thévenot, Delignette-Muller, Christieans, & Vernozy-Rozand,
differences between those values in the presence and absence of
2005). Our results are consistent with those of other authors
LM were statistically significant (TAPC, p ¼ 0.001; ENT, p ¼ 0.006;
(Salo, Ehavald, Raaska, Vokk, & Wirtanen, 2006; Talon et al., 2007),
and M&Y, p < 0.001). However, the standard deviations of each of
who also found persistence of TAPC, ENT, M&Y and LM after sani-
the parameters had a wide range. These results could be influenced
tizing non-food contact surfaces. Moreover, in our case, the places
by the fact that the number of positive results from the presence of
where LM was absent also showed a low level of TAPC, ENT and
LM was low despite the large number of samples analyzed.
M&Y.
The results for LM in this study were comparable with those
3.4. Description of the sites around the factory where LM was described in similar processing plants (Aguado, Vitas, & García-
located Jalón, 2004). In our case, the detection of LM was always repeated
in the same sampling places. This suggests that the presence of LM
Table 5 shows the locations where LM was detected. The fomites in certain niches could be determined by a) increased awareness
on the surfaces in contact with food, such as conveyor belts, among workers involved in cleaning activities of the negative
equipment and implements, etc, were included in Table 5, because consequences of the presence of micro-organisms on food contact
no positive results for the presence of LM were found on these. The surfaces, thus inducing them to carry out more vigorous cleaning of
sites that showed systematic presence of LM were the floor of the these; b) the existence of pools of water, condensation from
factory and objects in close contact with it (sanitary barrier, shoe refrigeration equipment or traces of water remaining on the floor
soles, equipment brackets, stair treads, small pools of water, etc). after clean-up operations. In food-processing areas, a final step is
We can emphasise the similarity of the values obtained before and carried out after sanitization, which consists of drying wet surfaces
after sanitizing in such locations, which are characterized by being with hand mops, but this is not applied to the floor or the base of
wet for long periods of time. the equipment.
Certain authors (Lundén, 2004; Wirtanen & Salo, 2004) stated
4. Discussion that LM represented a problem in the food industry because it was
especially present in refrigerated areas, fridges and freezers, as well
In the present study, surfaces in contact with foods were found as on floors and in drains. Similarly, in our study it was most often
to be free of LM, and its presence was not detected in any case after found on the floor and on shoe cleaning equipment. These are
sanitization. On the other hand, LM was occasionally detected on places that retain moisture thus allowing LM to multiply (Bell et al.,
some non-food contact surfaces, where the bacterium can survive, 2005). Thus, the process of drying the surfaces seems to be of great
always accompanied by the other three indicators of potential food importance for controlling microbial growth (Montville, Chen, &
microbial contamination (TAPC, ENT and M&Y). Schaffner, 2002). Moreover, the efficiency of cleaning and disin-
This study shows that both the cleaning and disinfection treat- fection products against LM is strongly influenced by the sort of the
ments (protocols A and B) assayed successfully reduced TAPC, ENT, food matrix present in the environment, and in most cases, it is
M&Y, and LM, and that a significant reduction of the presence of reduced by the presence of food debris (Chaitiemwong, Hazeleger,
these microbial indicators was found before and after cleaning of & Beumer, 2010; Gram, Bagge-Ravn, Ng, Gymoese & Vogel, 2007).
the food or non-food contact surfaces. However, there are some After assessing the results, given the survival of LM in cold and wet
environments, such as the floor and objects in contact with it, the
Table 4 latter should be considered the reservoir for LM and other potential
TAPC, ENT, and M&Y according to the presence or absence of LM. hazardous micro-organisms that can contaminate foods by bio-
aerosol formation, and should therefore be included within the
Parameter measured Presence of LM Absence of LM Significance
good-hygiene practices and HACCP systems (Christison, Lindsay, &
Mean  SD (n) Mean  SD (n) p von Holy, 2008; Legnani, Leoni, Berveglieri, Mirolo, & Alvaro, 2004;
TAPC (cfu/cm2) 8.7  4.9 (16) 4.6  5.3 (111) 0.001 Sharma & Anand, 2002; Reij & Den Aantrekker, 2004). Various
ENT (cfu/cm2) 2.5  3.1 (16) 1.3  2.7 (111) 0.006
authors (Aarnisalo, Tallavaara, Wirtanen, Maijala, & Raaska, 2006;
M&Y (cfu/cm2) 3.9  4.1 (18) 1.4  2.2 (129) <0.001
Bell & Kyriakides, 2005; Cox et al., 1989; Fuster-Valls, Hernández-
Results are expressed as mean  standard deviation (SD). Herrero, Marín-de-Mateo, & Rodríguez-Jerez, 2008) have already
cfu/cm2: colony forming units by area (in square centimetres).
TAPC: total aerobic plate count; ENT: Enterobacteriaceae count; and M&Y: mould
highlighted the importance of rapid drying of wet surfaces after
and yeast count; LM: Listeria monocytogenes. cleaning and disinfection when the manufactured processes were
n: number of samples; p: significance level between presence and absence LM. completed, because this helps to reduce the proliferation of
Author's personal copy

30 M. Campdepadrós et al. / Food Control 23 (2012) 26e31

bacteria as water is an essential factor for microbial growth and the Fuster-Valls, N., Hernández-Herrero, M., Marín-de-Mateo, M., & Rodríguez-Jerez, J. J.
(2008). Effect of different environmental conditions on the bacteria survival on
formation of biofilm. However, the resistance of LM could also be
stainless steel surfaces. Food Control, 19(3), 308e314.
due to inefficient cleaning with remnants of organic material Garrido, V., Torroba, L., García-Jalón, I., & Vitas, A. I. (2008). Surveillance of listeriosis
remaining. Thus, persistent organic matter could be removed in Navarre, Spain, 1995e2005 -epidemiological patterns and characterisation of
physically by chemical sanitising products (adsorption and clinical and food isolates. Euro Surveillance, 13(49), 1e6.
Gram, L., Bagge-Ravn, D., Ng, Y. Y., Gymoese, P., & Vogel, B. F. (2007). Influence of
absorption phenomena) or chemically (by redox phenomena), thus food soiling matrix on cleaning and disinfection efficiency on surface attached
reducing their biocide activity. Listeria monocytogenes. Food Control, 18(10), 1165e1171.
The present study highlights the specific locations where LM is Inoue, S., Nakama, A., Arai, Y., Kokubo, Y., Maruyama, T., Saito, A., et al. (2000).
Prevalence and contamination levels of Listeria monocytogenes in retail foods in
able to survive in a food-processing factory, thus enabling efforts to Japan. International Journal of Food Microbiology, 59(1e2), 73e77.
be concentrated on sanitizing these places. In addition, it is ISO 18593. (2004). Microbiology of food and animal feeding stuffs e Horizontal
important to note that infrastructure changes could be useful for methods for sampling techniques from surfaces using contact plates and swabs.
Geneva: International Organization for Standardization.
reducing the presence of potential human pathogens by reducing ISO 4833. (2003). Microbiology of food and animal feeding stuffs - Horizontal method
water condensation and ponding, while making cleaning and for the enumeration of microorganisms - Colony-count technique at 30 degrees C.
disinfection easier (Miettinen, Björkroth et al., 1999). Finally, note Geneva: International Organization for Standardization.
ISO 5552. (1997). Microbiology of food and animal feeding stuffs - Horizontal methods
that the results obtained through sanitization protocol B, although for the detection and enumeration of Enterobacteriaceae - Part 2: Colony-count
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