FEMS Microbiology Letters 210 (2002) 271^275
www.fems-microbiology.org
Ecology of Listeria monocytogenes in the environment of raw poultry
meat and raw pork meat processing plants
Elise Chasseignaux a , Pascale Ge¤rault b , Marie-The¤re'se Toquin a , Gilles Salvat a ,
Pierre Colin a , Gwennola Ermel a;
a
AFSSA Ploufragan, Research Unit of Hygiene and Quality of Poultry and Pork Products, Zoopole Beaucemaine, BP 53, 22 440 Ploufragan, France
b
AFSSA Ploufragan, Research Unit of Swine Epidemiology and Quality Assurance, Zoopole Les Croix, BP 53, 22 440 Ploufragan, France
Received 10 September 2001; received in revised form 15 March 2002; accepted 19 March 2002
First published online 25 April 2002
Abstract
The zoonotic Listeria monocytogenes is mainly transmitted to humans by the food-borne route. This bacterium was often found in the
environment of food processing plants. Therefore the aims of this study were (i) the identification of environmental factors associated with
L. monocytogenes contamination on working and non-working surfaces in poultry or pork processing plants and (ii) the understanding of
its survival in such environments. The physicochemical risk profiles showed that a surface in resin or plastic, rather than uneven, with
organic residues, with a neutral pH, a low temperature and a high hygrometry was associated with L. monocytogenes
contamination. 2 2002 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
Keywords : Ecology; Poultry; Pork; Processing plant environment; Listeria monocytogenes
1. Introduction
Listeria monocytogenes has been described as one of
the major human food-borne pathogens. Listeriosis can
occur as a sporadic disease or as an outbreak and is often
related to the consumption of contaminated food. In
France, during the last 10 years, di¡erent outbreaks
were associated with either delicatessen (pork tongue
in jelly in 1992 [1], pork ‘rillettes’ in 1993 [2] and 1999^
2000 [3]) or soft cheeses (‘Brie de Meaux’ in 1995 [4],
‘Pont l’Eve“que’ and ‘Livarot’ in 1997, ‘Epoisses’ in 1999
[3]). Di¡erent studies on L. monocytogenes prevalence
showed that 16% of raw pork meat and 17% of raw
poultry meat were contaminated [5]. The plant environment can also be contaminated : about 8% of samples in
poultry slaughterhouses [6], 26% of samples in raw poultry meat plants [7] and 68% of samples in raw pork meat
plants [8].
* Corresponding author. Tel. : +33(2)96 016 287;
Fax : +33(2)96 016 283.
E-mail address : [email protected] (G. Ermel).
Therefore, the understanding of the survival of
L. monocytogenes isolates is essential to prevent contamination in food plant environments. Actually, despite
some studies on the tracing of L. monocytogenes in
processing plants [9^12], to our knowledge the associated
environmental risk factors of this microorganism are
not completely analysed. Generally, ecological and physiological data came from laboratory experiments:
L. monocytogenes could generally grow from 1 to 45‡C
[13], even if some strains can develop at 0.5‡C [14] or at
30.2‡C [15]. L. monocytogenes isolates could grow from
pH 5.0 to 9.6; however, the optimal pH is neutral to
slightly alkaline [16]. All these assays were realised with
arti¢cial media, therefore some nutriments or inhibitory
substances found in natural environments could be missing.
The aim of this study was to identify the environmental risk criteria associated with L. monocytogenes colonisation on working and non-working surfaces in ¢ve
processing plants: two of raw poultry (A and B) and three
of raw pork meat (C, D and E). These surfaces were
considered as the main source of meat contamination.
The link between risk factors and physicochemical characteristics of the surfaces was studied by statistical analysis.
0378-1097 / 02 / $22.00 2 2002 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved.
PII : S 0 3 7 8 - 1 0 9 7 ( 0 2 ) 0 0 6 3 7 - 7
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2. Materials and methods
2.1. Plants studied
Two poultry (A and B) and three pork (C, D and E)
meat processing plants were studied. Plants A, B, C and D
are in the North West of France whereas plant E is in the
South East. The plants were divided into three di¡erent
areas : reception of raw materials, meat processing and
product processing. The working rooms were studied during the processing or after the cleaning operations at different times: 1 year (plant A), over 4 months (plant C),
2 months (plants B and D) and only one visit (plant E).
2.2. Swabbing
The sampling surfaces were grouped into two classes:
(i) the environment for the surfaces without any contact
with the raw meat (£oor, wall, sewer) and (ii) the equipment for the surfaces in direct contact with the raw meat
(working table, transport belt, knives, etc.). The swabbing
was delimited with a sterile stainless steel frame (a surface
of 162.5 cm2 ) using a tissue swab moistened with 5 ml
tryptone salt, 10% (v/v) Isobio0 (Laboratoire LCB,
Lugny, France). Isobio0 is used to neutralise cleaning
products and disinfectants.
For each swabbing, di¡erent data were collected concerning the surface : composition (plastic, resin, stainless
steel, metal, painted metal, tiling, cement or painted cement), cleanness (clean, presence of organic residues, presence of dust, presence of organic grease or encrustation),
visual status (smooth, granular, stripped or damaged),
moisture (dry surface, moisture or presence of water), temperature and pH of the surface. Surface temperature was
measured using a thermocouple thermometer and the surface pH was determined using pH indicator paper. Room
temperature and hygrometry were also collected using a
digital hygrometer.
2.3. L. monocytogenes detection procedure
The tissue swab was resuspended in 90 ml half Fraser
broth (bioMe¤rieux, Marcy l’Etoile, France) and incubated
at 30‡C. After 24 h, each sample was streaked on Palcam
agar (bioMe¤rieux, Marcy l’Etoile, France) and incubated
for 48 h at 37‡C. The Vidas test (bioMe¤rieux, Marcy
l’Etoile, France) was then performed with typical colonies
on Palcam agar plates. The plates were soaked with 3 ml
tryptone salt broth and scraped. The obtained bacterial
suspension was used to perform the Vidas test according
to the manufacturer’s recommendations and to our own
validated protocol [17].
2.4. Statistical analysis
For each plant, an identical data analysis was per-
formed. The dependent binary variable LIST was coded
1 if the swab was positive for L. monocytogenes; otherwise
it was coded 0. Eleven independent environmental and
physicochemical variables were listed. They were divided
into two groups. The ¢rst group was composed of the
variables for the room conditions (room, sampling surface,
activity or cleaning operation) and the second group corresponded to the physicochemical and environmental conditions (composition, cleanness, visual state, moisture,
temperature and pH of the surface, temperature and hygrometry of the room).
Frequencies were calculated for all the qualitative variables, and minima and maxima were noted. Histograms
were drawn for all the quantitative variables and the
mean, standard deviation, median and quartiles were calculated. Each quantitative variable was split into separate
classes depending on our biological and microbiological
knowledge. The class numbers were not under 10% of
the swabs. Relationships between LIST and each of the
other variables were then assessed in two-by-two tables
and tested with the chi-square method. During this ¢rst
screening, variables statistically associated with LIST
(P 9 0.15) were retained. Tests between independent variables were also performed so that redundant variables
were eliminated.
Multiple correspondence analyses (MCA) were then
performed using the software SPAD-N. The data of group
2 retained after the chi-square tests were active whereas
the variables of group 1 retained after the second phase
were illustrative. Successive MCA were performed and the
variables with the highest inertia on the ¢rst axes were
retained. Then the proximity between LIST+, LIST3
and the modalities of the other variables were studied.
3. Results and discussion
3.1. Detection of L. monocytogenes
The examination of the 497 samples, of which 263 were
realised during activity and 234 after the cleaning operations, showed that 23.7% of the samples were contaminated by L. monocytogenes. Table 1 indicates the contamination in the di¡erent plants either in the environment or on
the equipment of the di¡erent studied rooms.
During processing, 38% of the samples contained
L. monocytogenes, 38.9% in the poultry processing plants
and 37% in the pork processing plants. This contamination was higher than that observed by Lawrence et al. [7]
in a raw poultry meat processing plant (26%) but lower
than that noticed by Salvat et al. [8] in a raw pork plant
(55%). Nevertheless it was heterogeneous in the di¡erent
plants. Two cases were beheld: an overall contamination
either in the environment (plants A and B) or on the
equipment (plants C, D and E). However, di¡erences
were observed when the di¡erent rooms were considered.
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273
Table 1
Distribution of the 497 swabbing samples regarding L. monocytogenes contamination in the ¢ve plants (A^E) in the environment or on the equipment
of the di¡erent workrooms during activity and after cleaning
Plant
Type of swabbing
Number of samples contaminated by L. monocytogenes/total number of samples
Reception
A
B
C
D
E
Environ.
Equip.
Environ.
Equip.
Environ.
Equip.
Environ.
Equip.
Environ.
Equip.
Meat processing
Product processing
Total
Act.
Cle.
Act.
Cle.
Act.
Cle.
Act.
Cle.
9/17 (53%)a
1/3 (33%)
4/4 (100%)
0/2 (0%)
1/6 (16.5%)
0/3 (0%)
0/4 (0%)
Xb
0/3 (0%)
1/1 (100%)
11/27 (41%)
0/3 (0%)
ND
ND
0/5 (0%)
0/5 (0%)
0/4 (0%)
X
0/3 (0%)
0/1 (0%)
2/5 (40%)
15/18 (83%)
8/12 (66.5%)
0/4 (0%)
0/11 (0%)
18/23 (78.2%)
1/3 (0%)
4/11 (36.3%)
1/4 (25%)
7/7 (100%)
0/7 (0%)
0/32 (0%)
2/8 (25%)
0/2 (0%)
0/11 (0%)
0/19 (0%)
0/3 (0%)
0/11 (0%)
1/4 (25%)
0/6 (0%)
7/14 (50%)
7/51 (13.7%)
3/8 (37.5%)
0/6 (0%)
0/6 (0%)
1/9 (11%)
2/4 (50%)
5/8 (62.5%)
3/8 (37.5%)
0/7 (0%)
0/6 (0%)
0/24 (0%)
2/8 (25%)
0/6 (0%)
0/5 (0%)
(0%) (7.1%)
0/4 (0%)
0/9 (0%)
1/8 (12.5%)
0/7 (0%)
18/36 (50%)
23/72 (31.9%)
15/24 (62.5%)
0/12 (0%)
1/23 (4.4%)
19/35 (54.3%)
2/11 (18.2%)
10/20 (50%)
4/15 (26.5%)
8/15 (53.3%)
11/40 (27.5%)
0/50 (0%)
4/16 (25%)
0/8 (0%)
0/21 (0%)
1/38 (2.6%)
0/11 (0%)
0/20 (0%)
2/15 (13.3%)
0/15 (0%)
Act., during activity; Cle., after cleaning; Environ., environment (£oor, wall, sewer) ; Equip., equipment (for example, working table, transport belt,
etc.) ; ND, not determined.
a
Percentage of positive samples.
b
X, no equipment present in this room.
In plant A, the environments of the reception and the
product processing areas were the most contaminated
(mostly on £oors) whereas the contamination was present
on the equipment of the meat processing area. In plant B,
only the environments of all areas were contaminated
(only on £oors). In plants C and D, the environment of
the reception area was colonised, and during meat and
product processing the contamination was more important
on the equipment (working tables, transport belts, etc.).
However, in plant E, L. monocytogenes was detected on
the equipment of the reception and meat processing areas
and in the environment of the product processing workroom.
After the cleaning operations, the contamination was
subsequently lowered (7.7%), with 13.1% in the poultry
plants. This result is similar to those obtained by Salvat
et al. [8]. In the pork plants, the contamination was
slightly lower (2.5%). The residual contamination was
mainly observed in the environments of plants A, B, and
E: 27.5%, 25% and 13.3%, respectively, of contaminated
swabs were found. On the contrary, in plant C, no contamination remained in the environment whereas one
equipment was still contaminated. In plant D, no remaining contamination was detected in either kind of swabbing. This could be due to distinct cleaning habits: alternative utilisation of two di¡erent cleaning products
whereas the other plants always used the same one. Therefore, in these other plants, some bacteria could develop a
resistance against the used cleaning product, survive and
eventually grow [18].
3.2. Pro¢les of risk factors for the environmental and
physicochemical variables
Each plant was studied separately. Table 2 presents the
characteristics of the surfaces and workrooms in the pres-
ence or absence of L. monocytogenes contamination. For
some parameters, the results were not conclusive, meaning
that no real di¡erence was observed for the variable in
either the presence or the absence of a contamination.
However, the global analysis of the di¡erent parameters
showed a convergence for some of them between the different plants whereas only inclinations or even divergences
were observed in other cases.
Convergence was observed for the cleanness of the surface and the hygrometry of the room. A clean surface was
associated with the absence of a contamination in almost
all plants (A, C, D and E) even if the presence of dust was
also recorded in plants A and E. However, in each plant
organic residues were noticed on the surface in case of a
L. monocytogenes detection.
In the absence of L. monocytogenes contamination, the
hygrometry of the workrooms was below 70%, whereas in
the presence of a contamination a higher hygrometry was
observed (from 70 to 80% in plants B, C, E and even
above 80% in plant A). However, no conclusion could
be drawn for plant D, as during activity the hygrometry
was always below 70% and conversely after the cleaning
operations it was always above 80%. Helke et al. [19]
observed a higher survival of L. monocytogenes in bio¢lm
at 75.5% of relative humidity than at 32.5%.
Inclinations were observed for the status, the pH and
the temperature of the surface and for the temperature of
the workrooms. A smooth surface was clearly linked with
the absence of L. monocytogenes detection. However,
when L. monocytogenes was detected, the surface was uneven: granular (plants A and B), stripped (plant D) or
damaged (plant C).
A pH under 6 was frequently associated with the absence of L. monocytogenes. However, when L. monocytogenes was detected, di¡erences in pH were noted but
nevertheless close to neutral (a pH from 6 to 6.5 was
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Table 2
Characteristics of the surfaces and workrooms in the absence or presence of L. monocytogenes contamination in the ¢ve plants studied
Absence of L. monocytogenes contamination
Surface
Workroom
Nature
Cleanness
State
Moisture
pH
Temperature
Temperature
Hygrometry
Plant A
B
C
D
E
stainless steel
clean or PD
smooth
dry
66
10^13‡C
8^12‡C
6 80%
stainless steel
NC
smooth
dry
6 6.5
s 20‡C
s 10‡C
6 70%
stainless steel; tiles
clean
smooth
moist
66
6 7‡C
6 8‡C
6 70%
NC
clean
smooth
moist
NC
s 8‡C
s 4‡C
NC
cement ; tiles
clean or PD
NC
dry
66
s 12‡C
s 10‡C
6 70%
Presence of L. monocytogenes contamination
Surface
Workroom
Nature
Cleanness
State
Moisture
pH
Temperature
Temperature
Hygrometry
Plant A
B
C
D
E
resin
POR
granulous
moist
6.5^8
6 7‡C
6 8‡C
s 80%
resin
NC
granulous
moist
s 6.5
6 10‡C
6 10‡C
70^80%
plastic
PORD
damaged
dry
6^6.5
10^13‡C
8^12‡C
70^80%
NC
PORG
stripped
dry
NC
6 8‡C
6 4‡C
NC
plastic
POR
NC
moist
6^6.5
6 12‡C
5^10‡C
70^75%
NC, not conclusive ; PD, presence of dust; POR, presence of organic residues; PORD, presence of organic residues and dust; PORG, presence of organic residues and grease. Results of the MCA: plant A (axis 1 (20.14%), axis 2 (16.49%), axis 3 (12.27%)), plant B (axis 1 (19.86%), axis 2 (17.94%),
axis 3 (15.94%)), plant C (axis 1 (27.62%), axis 2 (15.32%), axis 3 (13.89%)), plant D (axis 1 (26.55%), axis 2 (21.64%), axis 3 (16.58%)), plant E (axis 1
(22.85%), axis 2 (19.06%), axis 3 (15.34%)).
linked with the contamination in plants C and E, whereas
for plant A it was from 6.5 to 8, and for plant B above
6.5). This is in agreement with the growth characteristics
of L. monocytogenes, whose optimal pH is neutral to
slightly alkaline [16].
Regarding the temperature of the surface, di¡erences
were observed. In the absence of contamination, the surface temperature seemed rather high, above 10‡C (above
4‡C in plant D, between 10‡C and 13‡C in plant A, above
12‡C in plant E and above 20‡C in plant B). The only
exception was observed in plant C where the temperature
was either below 8‡C or above 13‡C. On the contrary,
when L. monocytogenes was detected, the temperature
was low, below 10‡C. However, in plant C the temperature was between 10‡C and 13‡C but the contamination
was still associated with the refrigerated temperature. The
same results were obtained for the room temperatures : the
temperature was rather high in the absence of L. monocytogenes contamination and inversely low in the presence
of a contamination. This result was expected as the surface
temperature was partly in£uenced by the room temperature. This was in agreement with the psychrotrophic properties of L. monocytogenes : this ability could select
L. monocytogenes while other competitive micro£ora could
not grow [16,20]. On the contrary, at high temperature,
the micro£ora could compete with L. monocytogenes, outnumber it, and therefore not allow its implantation. Moreover, our study con¢rmed the results of Helke et al. [19],
which showed a higher survival when the bio¢lm was at
6‡C compared to 25‡C with a relative humidity of 75.5%.
In our study, L. monocytogenes contamination was found
with low temperature and high hygrometry and, conversely, no contamination with high temperature and
low hygrometry.
Finally, for the nature and the moisture of the surface,
divergences were observed. When no L. monocytogenes
was detected, the surface was of stainless steel (plants A,
B and C), tiles (plants C and E) or cement (plant E). When
a contamination was observed, the surface was composed
of either resin (plants A and B) or plastic (plants C and E).
Nevertheless, this was in agreement with the surface state :
smooth in the absence of L. monocytogenes detection and
granular, stripped or damaged with L. monocytogenes contamination. Moreover, in the di¡erent studied plants, the
resin was used on the £oor as a non-skid surface and
therefore it was granular. On plastics, pits and cracks resulted of their use. Thus, for both surface kinds, microspaces existed, unreached by disinfectants, where soil and
bacteria could persist. Wong [21] also supported that hypothesis. Moreover, di¡erent studies related to bio¢lms on
stainless steel showed that nutrients could either enhance
or inhibit a bio¢lm of L. monocytogenes [19,22,23]. In our
study, this surface was found smooth or lightly stripped
and associated with the absence of contamination by
L. monocytogenes. Therefore, organic meat residues could
limit the establishment of L. monocytogenes bio¢lm on
stainless steel.
Concerning the moisture of the surface, a dry surface
was found in three plants (A, B and E) whereas a moist
surface was found in two plants (C and D) with no detec-
FEMSLE 10457 23-5-02
E. Chasseignaux et al. / FEMS Microbiology Letters 210 (2002) 271^275
tion of L. monocytogenes. Opposite results were noticed
when L. monocytogenes was detected. Therefore, no conclusion can be expressed for that criterion.
As a conclusion, the physicochemical risk pro¢les
showed that a surface in resin or plastic, therefore rather
uneven, with organic residues, with a neutral pH, a low
temperature and a high hygrometry was associated with
L. monocytogenes contamination. Now, it could be interesting to consider the accompanying £ora found in either
the presence or the absence of L. monocytogenes contamination. Indeed, as well as physicochemical factors, £ora
could also in£uence the surface colonisation by L. monocytogenes.
[7]
[8]
[9]
[10]
[11]
Acknowledgements
The authors acknowledge the Ultra-propre Nutrition
Industrie Recherche group for ¢nancial support for the
investigations, the French Ministe're de l’Education Nationale, de la Recherche et de la Technologie and the Agence
Nationale pour la Recherche et la Technologie (ANRT)
for its grant. The authors also acknowledge Y. Le No“treMichel, F. Eono and S. Gorin for their technical help
during the study.
[12]
[13]
[14]
[15]
[16]
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