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A seven-year survey of Campylobacter contamination in
meat at different production stages in Belgium
Y. Ghafir a,b,⁎, B. China b, K. Dierick c, L. De Zutter d, G. Daube b
a Belgian National Reference Laboratory in Food Microbiology for the Federal Agency for the Safety of the Food Chain, University of Liege,
Faculty of Veterinary Medicine, Department of Food Sciences, Microbiology, Bat. B43b, Sart Tilman, 4000 Liege, Belgium b University of Liege, Faculty of Veterinary Medicine, Department of Food Sciences, Microbiology, Bat. B43b, Sart Tilman, 4000 Liege, Belgium
c Scientific Institute of Public Health, rue Juliette Wytsman, 14, 1050 Brussels, Belgiumd University of Gent, Faculty of Veterinary Medicine, Food Microbiology, Salisburylaan, 133, 9820 Merelbeke, Belgium
Received 3 July 2006; received in revised form 3 November 2006; accepted 14 December 2006
Abstract
The presence of Campylobacter was assessed in different samples of poultry, pork and beef meat and carcasses from slaughterhouses,
production plants and retail level. An introductory study from 1997 to 1999, had the purpose of establishing the optimum dilution to detect
changes in prevalence and allowed a semi-quantitative estimation of poultry and pork contamination. Following this, between 2000 and 2003,
4254 samples were taken in order to study the trends. The poultry matrixes represented the greatest number and the most highly contaminated
samples, with 30.9% (in 0.01 g) positive samples, 18.7% (in 1 g), 46.9% (in 25 g) and 19.6% (in 0.01 g) for broiler carcasses, broiler fillets,
prepared chicken and layer carcasses, respectively. Broiler carcasses and fillets sampled at retail level were significantly less contaminated than
samples from production plants. Pork, beef and veal samples were rarely contaminated and, where contamination existed, it was at a low
prevalence (maximum 5.0%). The high and unvarying prevalence of Campylobacter in poultry necessitates the implementation of intervention
measures at the primary production level, in addition to methods of minimizing cross-contamination at the processing level. A survey plan in linewith the present study could be used in the future to monitor the effects of the planned measures and performance objectives and to follow the
evolution of Campylobacter contamination at all stages of the food chain, in accordance with European legislation.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Foodborne pathogens; Campylobacter ; Meat; Poultry; Pork; Beef
1. Introduction
In industrialized countries, Campylobacter and Salmonella
are the most frequent causes of acute bacterial enteritis (Butzler,
2004). In Europe, the number of reported cases of campylo- bacteriosis increased consistently between 1993 and 2002. Most
cases are sporadic (Tirado and Schmidt, 2001). In 2003, the 11
reporting member states of the European Union registered 48.9
cases of campylobacteriosis per 100,000 of the population. In
Belgium, this pathogen is the second highest cause of bacterial
gastro-enteritis in terms of reported incidence by the public
health services; 63.8 cases of human campylobacteriosis per
100,000 people were reported by the National Reference and
the Sentinel Laboratories in 2003 (Anonymous, 2005b). In theUnited States, 12.6 cases of campylobacteriosis per 100,000
people were reported in 2003 (CDC, 2004).
Food, and particularly poultry, is involved in about 80% of
cases of human campylobacteriosis (Mead et al., 1999; Butzler,
2004; Keener et al., 2004). Several studies have shown Cam-
pylobacter contamination of faecal samples from beef, pork and
poultry, of meat from pork, beef, turkey, shellfish, and of
sheep's liver (Zanetti et al., 1996; Endtz et al., 1997; Mayrhofer
et al., 2004; Whyte et al., 2004; Boes et al., 2005; Cornelius
et al., 2005). Consumption of inadequately treated water, raw
milk and various meats, in addition to contact with pets and
International Journal of Food Microbiology 116 (2007) 111 – 120
www.elsevier.com/locate/ijfoodmicro
⁎ Corresponding author. University of Liege, Faculty of Veterinary Medicine,
Department of Food Sciences, Microbiology, Bat. B43b, Sart Tilman, 4000
Liege, Belgium. Present address: Federal Agency for the Safety of the Food
Chain, WTCIII, 30 bd S. Bolivar, 1000 Brussels, Belgium. Tel.: +32 2 208 36
25; fax: +32 2 208 33 37.
E-mail address: [email protected] (Y. Ghafir).
0168-1605/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.ijfoodmicro.2006.12.012
mailto:[email protected]://dx.doi.org/10.1016/j.ijfoodmicro.2006.12.012http://dx.doi.org/10.1016/j.ijfoodmicro.2006.12.012mailto:[email protected]
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farm animals, have been implicated in outbreaks of campylo-
bacteriosis (Frost, 2001).
A European Directive 2003/99/EC on the monitoring of
zoonoses and zoonotic agents included campylobacteriosis
and Campylobacter spp. amongst the zoonotic agents to be
monitored by Member States at the level of primary production
and/or at other stages of the food chain (Anonymous, 2003). Ascientific panel from the European Food Safety Agency (EFSA)
has highlighted the need for more qualitative and quantitative
data on the occurrence of Campylobacter in food production
chains, particularly poultry (Anonymous, 2005a).
Our research was undertaken in Belgium. The prevalence of
Campylobacter in poultry, pork and beef meat was monitored
between 1997 and 2003 and focused on thermophilic Campy-
lobacter (Campylobacter jejuni and Campylobacter coli). The
introductory study took place from 1997 to 1999 when the
number and dilution of samples to be analysed were assessed. In
the second part of the study, from 2000 to 2003, the prevalence
of Campylobacter was evaluated at all production stages fromcarcasses at the slaughterhouse to the retail level. The objectives
of the whole study were (i) to assess the prevalence of Cam-
pylobacter at the different stages through the pork, poultry and
beef meat production chains, (ii) to gain a semiquantitative
estimation of the levels of contamination, and (iii) to evaluate
the changes in prevalence over the course of time.
2. Materials and methods
2.1. Sampling plan
From 1997 to 1999, a preliminary monitoring plan was used
to assess the prevalence of Campylobacter of carcasses and of cuts, liver and minced meat from pork, beef and veal, and of
carcasses and fillets from poultry, rabbit and turkey. Fishes from
aquaculture were also tested during this period. These samples
were chosen either because studies had shown that these
foods contained Campylobacter , or as a means of assessing its
prevalence in most types of meat produced in Belgium. All
these samples were obtained from several Belgian production
plants. For beef and pork, there were approximately 110
slaughterhouses (of which 40 of those for pork and 40 for beef
were high capacity establishments), and more than 1000
production plants for cuts, meat products and ground meat.
The total number of poultry establishments consisted of approximately 40 abattoirs (of which 25 were high capacity
slaughterhouses) and 125 cutting plants. Between 1997 and
1999, carcasses and livers from beef, pork and poultry were
sampled in slaughterhouses. Minced meat, cuts and fillets from
beef, pork and broilers were collected in production plants. The
choice of sampling location was made by the sampler in his area
of work. During this period, some of the big plants were over-
represented. The number of different establishments visited was
1 to 11 in 1997, 1 to 26 in 1998, and 7 to 36 in 1999 for each
type of sample.
Between February 2000 and December 2003, a new sam-
pling plan was implemented to allow representative sampling
of the entire Belgian meat production process, including the
retail level (butcheries and supermarkets). Carcasses, trimmings
and/or minced meat from pork, beef and poultry were sampled
from slaughterhouses, processing plants and/or retail establish-
ments for 10 to 11 months per year. The number of samples
taken at the production level was proportional to the capacity of
the establishment (number of carcasses slaughtered or quantity
of meat produced during a year), and took into account therepresentative distribution of production in all Belgian regions.
The largest production plants were sampled each year. The retail
and low capacity establishments (producing a limited number of
carcasses or meat for the Belgian domestic market) were
randomly chosen and often changed from year to year.
Each year, 300 samples per meat type were chosen to make
up the majority of the samples. This number of samples was a
compromise to achieve a small confidence interval around the
observed prevalence in order to detect a reduction in Campy-
lobacter 's true prevalence. In the case of layers, 100 to 200
carcasses were sampled each year because, since 2000, only 4
slaughterhouses have been responsible for processing morethan 200,000 layer carcasses each year, for an annual Belgian
production of 20 to 32 millions carcasses.
During the introductory study from 1997 to 1999, Campy-
lobacter were detected in pork and poultry samples in the main
suspension and in two or three dilutions of the initial suspension
(1/25, 1/250 and/or 1/2500). According to these results, the
dilutions of samples to be analysed were reassessed, according
to the procedure of Ghafir et al. (2005), in order to clarify the
extent of the reduction in the prevalence of Campylobacter in
each meat type. For the most contaminated samples (broiler and
layer carcasses), the dilutions showing the lowest prevalence
(0.01 g) were chosen (Table 1). For chicken fillets, a dilution
corresponding to 1 g was chosen in line with the Salmonella
criteria for meat preparation, according to the European
Directive 94/65/EC (Anonymous, 1994). No dilution had to
be made for the less contaminated samples or for broiler
prepared meat (detection of Campylobacter in 25 g in pork,
beef and broiler prepared meat samples).
2.2. Sample collection
The sampling was performed according to the procedure of
Ghafir et al. (2005). The following samples consisted of swabs
taken between 2 h and 4 h after slaughtering: pork (600 cm2),
veal (400 cm2
), beef (400 cm2
) and rabbit (400 cm2
) carcasses; pork (700 cm2), beef (400 cm2) and veal (400 cm2) liver. The
whole poultry carcasses and at least 200 g of minced meat, cuts
(small chops obtained at the end of the production process of
meat), fillets (boned breasts of chicken), or prepared meat (raw
ground meat processed as sausages or hamburgers sampled at the
retail level) were sampled at the end of the production process
(after chilling) and were placed in a sterile plastic bag. Layer
carcasses were reproductive hens and layers slaughtered after
egg production. At retail establishments, whole poultry packages
were taken. Turkey skin and chicken liver were sampled at the
slaughterhouse, and fishes were taken alive at the pisciculture.
Each sample was immediately put into an insulated refrigerated
box and was transferred the same day to the laboratory.
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2.3. Microbiological analyses and expression of results
Three laboratories licensed by the Belgian Ministry of Public
Health and accredited in accordance with the requirements of
the ISO 17,025 standard performed all the analyses. In the
laboratory, samples were stored chilled and were examined
within 24 h. The official SP-VG-M003 method from the
Ministry of Public Health was used for the detection of
thermophilic Campylobacter spp. (C. jejuni and C. coli). For
swabs, a 100 ml volume of Preston broth (nutrient broth no. 2
CM0067, Campylobacter selective supplement SR0117E and
lyzed horse blood SR0048, Oxoid, Basingstoke, England) was
added to the sterile plastic bag containing the swabs. For poultry
carcasses, 25 g of neck and breast skin from each carcass was
aseptically sampled in the laboratory and was homogenized
in 225 ml of Preston broth. The same sampling and dilution
Table 1
Campylobacter prevalence on carcasses and in meat from 1997 to 1999
Sampling level Dilution 1997 1998 1999 1997–1999
n a % b n a % b n a % b n a % b
Broilers
Carcasses 25 g 1/1 124 71.0 146 72.6 270 71.9
0.1 g 1/250 146 61.6 141 75.9 287 68.60.01 g 1/2500 141 58.9 141 58.9
Fillets 25 g 1/1 120 80.8 151 83.4 271 82.3
1 g 1/25 139 57.6 139 57.6
0.1 g 1/250 151 19.2 151 19.2
0.01 g 1/2500 139 19.4 139 19.4
Liver 25 g 1/1 120 61.7 142 74.6 262 68.7
0.1 g 1/250 142 72.5 142 72.5
Layers
Carcasses 25 g 1/1 120 91.7 141 82.3 261 86.6
0.1 g 1/250 141 73.0 122 90.2 263 81.0
0.01 g 1/2500 122 68.9 122 68.9
Turkey
Carcasses 25 g 1/1 120 72.5 150 86.7 270 80.4
0.1 g 1/250 150 26.7 150 26.7
Pork
Carcasses 600 cm2 1/1 80 16.3 150 15.3 153 19.0 383 17.0
24 cm2 1/25 153 8.5 153 8.5
2.4 cm2 1/250 150 2.0 150 2.0
Cutting meat 25 g 1/1 39 2.6 149 9.4 152 12.5 340 10.0
1 g 1/25 152 3.3 152 3.3
0.1 g 1/250 149 0.0 149 0.0
Minced meat 25 g 1/1 60 3.3 146 6.2 149 2.0 355 3.9
1 g 1/25 149 0.7 149 0.7
0.1 g 1/250 146 1.4 146 1.4
Liver 700 cm2 1/1 60 28.3 143 32.9 203 31.5
2.7 cm2 1/250 143 2.1 143 2.1
Beef
Carcasses 400 cm2 1/1 60 3.3 60 3.3
Cutting meat 25 g 1/1 60 5.0 60 5.0
Minced meat 25 g 1/1 67 0.0 67 0.0
Liver 400 cm2 1/1 60 31.7 60 31.7
Veal
Carcasses 400 cm2 1/1 59 0.0 59 0.0
Minced meat 25 g 1/1 58 0.0 58 0.0
Liver 400 cm2 1/1 60 11.7 60 11.7
Rabbit
Carcasses 400 cm2 1/1 120 4.2 120 4.2
Fish
Flesh 25 g 1/1 131 2.3 131 2.3
a Number of samples. b Prevalence of Campylobacter .
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methods were used for the other meat types. In order to detect
Campylobacter in 1 g, 0.1 g or 0.01 g (in 24 cm2, 2.4 cm2 or
2.7 cm2 for pork liver or carcasses), a dilution was made by
taking volumes of 10, 1 and 0.1 ml, respectively, from the main
suspension. These were transferred into a sterile tube, bag or
bottle, and 90 ml, 9 ml or 10 ml of sterile Preston broth was
added.Incubation of Preston for 17 to 19 h at 42 °C took place under
microaerophilic conditions (obtained either by expelling the
air from the bag and closing the bag just above the level of the
liquid (Hernandez, 1996; Mohammed et al., 2005) or by using
Campygen, CN0025 or CN0035, Oxoid, Basingstoke, England
or Genbag, BioMérieux, Marcy l'Etoile, France). Following
this, 0.1 ml was streaked onto an mCCDA plate (modified
charcoal deoxycholate agar, Campylobacter blood-free selec-
tive medium, CM0739 and CCDA selective supplement,
SR0155, Oxoid, Basingstoke, England) and was incubated for
24 to 120 h at 42 °C in a microaerophilic atmosphere. On 5
suspected isolates, biochemical (using API Campy, BioMér-ieux, Marcy l'Etoile, France) or genetic confirmation (Linton
et al., 1997; Vandamme et al., 1997) for the genus and the
species of Campylobacter was performed. The lowest limit
of detection was 1 CFU/25 g, 400 cm2 or 600 cm2 for a 25 g,
400 cm2 or 600 cm2 sample analysed, respectively; 25 CFU/
25 g or 600 cm2 for a 1 g or 24 cm2 sample analysed, respec-
tively; 250 CFU/25 g or 600 cm2 for a 0.1 g or 2.4 cm2 sample,
respectively, and 2500 CFU/25 g when a 0.01 g sample was
used for the analysis. This method was specially designed to
find thermophilic Campylobacter : C. jejuni and C. coli. Other
Campylobacter species are sometimes also found using this
method.
Campylobacter results were recorded as absence or presencein the sample; from 2000, the prevalence of Campylobacter was
assessed in 25 g of pork, beef and poultry minced meat, in 1 g of
chicken fillets, and in 0.01 g of neck skin for chicken and layer
carcasses.
Chi-squared tests were used to determine the significance of
differences in prevalence of the samples obtained over several
years. For comparison of tables with two rows and two
columns, Fisher's exact test was used. The confidence intervals
were calculated exactly using binomial distribution.
3. Results
The preliminary study carried out in 1997 and 1998 revealed
that the prevalence of Campylobacter in 25 g samples of
chicken and layer carcasses ranged from 71.9% to 86.6%,
respectively. The prevalence in these samples was very high:
more than 58% of the 0.01 g samples were positive in 1999. In
the 0.1 g and 0.01 g samples, chicken fillet was the poultry
product in this study that contained the lowest number of
Campylobacter cells (around 19%). In chicken liver and turkey
carcasses analysed in 1997 and 1998, the prevalence was,
respectively, of 68.7% and 80.4%, with 72.5% and 26.7% of
0.1 g samples still contaminated. These results are summarizedin Table 1.
For pork meat production, the prevalence rates were 17.0%,
10.0% and 3.9% on carcasses (600 cm2), trimmings (25 g) and
minced meat (25 g), respectively. In 1999, (when 24 cm2 or 1 g
samples were considered), the prevalence rates on carcasses and
trimmings and in minced meat were 8.5%, 3.3% and 0.7%,
respectively. For 2.4 cm2 or 0.1 g samples, the prevalence rates
were 2.0%, 0.0% and 1.4%, respectively. Campylobacter were
found in 31.5% of 700 cm2 samples of pork liver, but only in
2.1% of 2.7 cm2 samples.
For beef carcasses and cutting meat, only a very small
number of samples were contaminated with Campylobacter
(3.3% and 5.0%, respectively), but no positive result was foundfrom minced meat from beef and veal, or from veal carcasses.
Liver was the most contaminated sample from beef and veal,
with 31.7% and 11.7% on 400 cm2, respectively. For rabbit
carcasses and fish flesh samples, the prevalence was low, with
Fig. 1. Semiquantitative evaluation of Campylobacter contamination in pork and poultry meat according to prevalence results obtained from 1997 to 1999.
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4.2% and 2.3% of Campylobacter being found on 400 cm2 and
in 25 g, respectively. These results are summarized in Table 1.
During 1997, 1998, and 1999 the presence of Campylobacter
was assessed in three dilutions of most poultry and pork samples
(Fig. 1): in 25 g or on 600 cm2, in 1 g or on 24 cm2 (25 times
dilutions), in 0.1 g or on 2.4 cm2 (250 times dilutions) and/or in
0.01 g (2500 times dilution). The percentage of samples without
Campylobacter in 25 g corresponded to the percentage of
samples containing b1 CFU in 25 g for cumulative 3-year
results. For example, 71.9% of chicken carcasses contained
more than 1 CFU/25 g, i.e. 28.1% of chicken carcasses were
negative for Campylobacter . The estimation of the percentage of samples containing 1 to 249 CFU/25 g was the difference
between the prevalence of Campylobacter in 25 g and in 0.1 g
(3.2% of chicken carcasses with 1 to 249 CFU/25 g). The
proportion of samples with 250 to 2499 CFU/25 g corresponded
to the difference between the prevalence in 0.1 g and in 0.01 g
(9.8% of chicken carcasses with 250 to 2499 CFU/25 g), and the
prevalence of Campylobacter in 0.01 g corresponded to the
proportion of samples including more than 2499 CFU/25 g
(58.9% of chicken carcasses containing more than 2499 CFU/
25 g). For pork samples, the four categories were: (1) b1 CFU/
25 g or 600 cm2 (83.0% on pork carcasses), (2) between 1 and
24 CFU/25 g or 600 cm2 (8.5% on pork carcasses), (3) 25 to
249 CFU/25 g or 600 cm2 (6.5% on pork carcasses) and (4)
N249 CFU/25 g or 600 cm2 (2.0% on pork carcasses), using the
same approach. In order to compare the estimated levels of
contamination of poultry and pork samples, four and three
cumulative categories, respectively, were considered, as shown
in Fig. 1: (1) b1 CFU/25 g, or 600 cm2, (2) between 1 and249 CFU/25 g or 600 cm2, (3) N249 CFU/25 g or 600 cm2 for
pork samples; between 250 and 1499 CFU/25 g for poultry
samples, and (4) N2500 CFU/25 g for poultry samples.
These results (Fig. 1) allowed a semiquantitative estimation
of the contamination in pork and poultry meat in production,
indicating that broiler and layer carcasses had the highest
Table 2
Evolution of Campylobacter prevalence in pork, poultry and beef samples from 2000 to 2003
Sampling
level
Dilution 2000 2001 2002 2003 2000–2003
n a % b n a % b n a % b n a % b n a % b, c
Broiler
Carcasses 0.01 g 1/2500 289 33.9 281 27.0 258 34.9 286 28.0 1114 30.9 (28.2–33.7)
Fillets 1 g 1/25 275 22.5A 229 15.3B 230 18.3 241 17.8 975 18.7 (16.3–21.3)Prepared meat 25 g 1/1 79 49.4 98 44.9 177 46.9 (39.4–54.5)
Layers
Carcasses 0.01 g 1/2500 187 23.0C 192 19.3 117 20.5 102 12.8D 598 19.6 (16.5–23.0)
Pork
Minced meat 25 g 1/1 308 1.3 296 3.7 604 2.5 (1.4–4.1)
Beef
Minced meat 25 g 1/1 488 0.6 298 0.7 786 0.6 (0.2–1.5)
a Number of samples. b Prevalence of Campylobacter within the same type of sample that do not share a common letter within the same type of sample (A to B, C to D) are significantly
different ( P b0.05).c
Values are mean (values with 95% CI).
Fig. 2. Prevalence of Campylobacter in poultry and minced meat from pork and beef according to the sampling level (production or retail), based on cumulative results
from 2000 to 2003 (nprod: number of samples taken at production level; nret: number of samples taken at retail level). The columns with different letters (a, b, c and d)are significantly different within the same type of sample.
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Campylobacter contamination (58.9% and 68.9% contained
more than 2499 CFU/25 g, respectively). For broiler fillets,
63.1% of the samples contained between 1 and 249 CFU/25 g,
and 19.4% of fillets had a contamination level higher than
2499 CFU/25 g. Pork samples had a completely different
contamination pattern, with 83.0 to 96.1% of samples at
b1 CFU/25 g, and 3.3 to 8.5% of samples between 1 and24 CFU/ 25 g (or 600 cm2).
The second part of the study conducted from 2000 to 2003
(Table 2) revealed that, for all samples of poultry, pork and beef
origin, contamination with Campylobacter was stable during
that period ( P N0.05). This was the case for all except chicken
fillets and layer carcasses, which showed a reduction between
2000 and 2001 or between 2000 and 2003, respectively. The
cumulative prevalence was 30.9% for chicken carcasses (in
0.01 g), 18.7% for broiler fillets (in 1 g), 46.9% for prepared
broiler meat (in 25 g) and 19.6% on layer carcasses (in 0.01 g).
Pork and beef minced meat had the lowest rate of contamination
by Campylobacter : 2.5% and 0.6% of the samples were positive, respectively, in 25 g.
In the survey conducted from 2000 to 2003, the prevalence
of broiler carcasses and fillets was significantly higher at
production level (34.9% in broiler slaughterhouses and 22.1%
in cutting plants) in comparison with retail establishments
(20.5% for carcasses and 12.1% for broiler fillets in super-
markets and butcheries; P b0.0001). All broiler prepared meat
samples came from retail establishments, and layer carcasses
had the same prevalence rate (19.6%) at the two levels
( P N0.05) for the cumulative 4-year results. No significant
difference was observed between the samples collected in
minced meat production plants or from the retail level
(supermarkets and butcheries) for pork (2.1% and 2.7%,respectively) or beef (0.0% and 1.0%, respectively; P N0.05).
The prevalence rates of Campylobacter according to the
sampling level are shown in Fig. 2.
Between 2000 and 2003, the predominant species of Campy-
lobacter isolated from poultry, pork and beef in Belgium was
C. jejuni. The proportion of this species was 86.8% for chicken,
81.3% for layers, 75% for pork and 100% for beef. C. coli was the
second most frequently isolated species, with 10.5% to 16.7% of
isolates (except for beef, where only C. jejuni was detected). The
other isolated species from poultry and/or pork were Arcobacter
cryoaerophilus, C. lari, C. fetus and C. upsaliensis. These data
are summarized in Table 3.
4. Discussion
4.1. Sampling method
This study assessed the prevalence of Campylobacter in
poultry, pork, beef, veal and rabbit meat and carcasses, and in fish.
It was difficult to compare these results with other studies becauseof different samplingmethods, quantities analysed, sampling plan
and objectives. The samples used in most previous studies were
from poultry neck skin (Jorgensen et al., 2002; Moore et al., 2002;
Meldrum et al., 2005; Reiter et al., 2005), or were faecal or cloacal
samples (Oosterom et al., 1983c; Berndtson et al., 1996; Heuer
et al., 2001), swabs of carcasses (Miwa et al., 2003), liquid
exuded (Fernándes and Pisón, 1996), meat samples, or involved
techniques based on the rinse method of the whole poultry carcass
(Ledergerber et al., 2003; Stern et al., 2003). The quantity
analysedwasoften2.5g, 10g, 12g or 25g for meat, and 100 cm2
for swabs (Zanetti et al., 1996; Madden et al., 1998; Jorgensen
et al., 2002; Moore et al., 2002; Nesbakken et al., 2003; Pearceet al., 2003; Reiter et al., 2005) and the type of sample was not
always specifically mentioned (Fricker and Park, 1989; Padung-
tod et al., 2002; Pezzotti et al., 2003; Mayrhofer et al., 2004;
Whyte et al., 2004).
For the sampling of poultry carcasses, neck skin has been
chosen in the present study because it carries a higher risk of
Campylobacter contamination; during poultry slaughtering,
Campylobacter adhere to the skin, forming a biofilm, and can
be entrapped in ridges and crevices of the skin (Corry and
Atabay, 2001). In the United Kingdom, a study found no
difference between the isolation and enumeration methods for
Campylobacter using either neck-skin analysis (about 2.5 g
neck-skin) or the carcass-rinse method plus neck-skin sample(Jorgensen et al., 2002).
4.2. Prevalence and semiquantitative estimation of Campylo-
bacter contamination in 1997, 1998 and 1999
The results of the introductory study from 1997 to 1999
assessed the prevalence of Campylobacter in poultry (chicken,
layer and turkey), pork, beef, veal and rabbit meat and
carcasses, and in fish. Campylobacter spp. were found in 68
to 87% of 25 g poultry samples. Liver from pork, beef, and
especially chicken, was frequently found to be contaminated in
our study (31.5%, 31.7%, 68.7%, respectively), except for veal
Table 3
Main Campylobacter species isolated in pork, poultry and beef meat from 2000 to 2003
Chicken Layer Beef Pork Total
n a Proportion (%) n a Proportion (%) n a Proportion (%) n a Proportion (%) n a Proportion (%)
C. jejuni 446 86.8 87 81.3 5 100.0 9 75.0 547 85.7
C. coli 54 10.5 16 15.0 – – 2 16.7 72 11.3
A. cryoaerophilus 8 1.6 1 0.9 – – – – 9 1.4
C. lari 4 0.8 – – – – 1 8.3 5 0.8
C. fetus 2 0.4 1 0.9 – – – – 3 0.5
C. upsaliensis – – 2 1.9 – – – – 2 0.3
Total 514 100.0 107 100.0 5 100.0 12 100.0 638 100.0
a Number of isolates.
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liver (11.7%). Chicken liver was found to be less contaminated
in a comparable Brazilian study (Reiter et al., 2005), where
23.3% of samples were contaminated (in 25 g) at processing
level. In their study, Kramer et al. (2000) also found that ox and
pork livers were much more contaminated than red meat. The
high level of recovery of Campylobacter on the surface of the
liver is probably observed because this surface stays moist,which is a protective factor for this pathogen. For fish, a similar
prevalence rate to our result of 2.3% has been described in a
German study (Loewenherz-Lüning et al., 1996), probably due
to the contamination and resistance of Campylobacter in water
(Cools et al., 2003).
The analysis of different dilutions of samples during the
study from 1997 to 1999 allowed a semiquantitative estimation
of the contamination of poultry and pork meat production in
Belgium. Using the most probable number (MPN) method,
Dufrenne et al. (2001) found that 38% of contaminated chicken
carcasses (rinse method) contained b100 cells per carcass and
34% contained more than 1000 cells. Similarly, in the present study, 59% of chicken carcasses were found to contain more
than 100 Campylobacter per gram. In the Netherlands, a study
by Oosterom et al. (1983b) showed that 49% of chicken
carcasses (whole carcass samples) were positive for Campylo-
bacter , ranging from 2000 to 100,000 cells/carcass. In the
present study, broiler fillets showed a lower prevalence, with
80.8% containing fewer than 249 cells per 25 g, probably
because of the absence of skin on these samples. Pork carcasses
and meat had a prevalence rate of between 3 and 17% in
600 cm2 or 25 g samples, but Campylobacter were detected in 0
to 9% of the diluted samples. The prevalence of beef and veal
carcasses and meat was of a maximum of 5%.
4.3. Prevalence and changes between 2000 and 2003
The second part of our study, in the form of the survey
conducted from 2000 to 2003, was representative of the total
Belgian production of poultry, pork and beef meat during
that period. Except for prepared chicken meat, the samples
were taken from slaughterhouses, cutting plants and/or retail
establishments.
The mean prevalence of Campylobacter was 30.9% in
broiler carcasses (0.01 g samples) and 18.7% in broiler fillets
(1 g samples). This means that 30.9% of broiler carcasses
contained more than 100 CFU/g. Layer carcasses were muchless contaminated (19.6% in 0.01 g samples) than chicken
carcasses in the present study. Similar results were observed in
another Belgian study (Uyttendaele et al., 1999), which found
Campylobacter in 25.6% and 21.9% of chicken and layer
carcasses (in 100 cm2 of skin) from a Belgian supermarket
depot. The lower results for layers in comparison with broilers
could be due to the freezing of some layer carcasses, which is a
common practice at production establishments. Retail establish-
ments are known to sell layers after thawing. Campylobacter
prevalence is known to be significantly lower after thawing
(Oosterom et al., 1983a). Prepared poultry meat, corresponding
to raw ground meat processed as sausages or hamburgers,
sampled at the retail level, was much less contaminated (46.9%
in 25 g samples analysed in 2002 and 2003) than chicken
carcasses and fillets analysed at production level from 1997 to
1999 in 25 g (71.9% and 82.3% in 25 g samples, respectively).
Uyttendaele et al. (1999) found only 6.4% (25 g) positive
samples for processed chicken products, including sausages and
barbecue products at retail level.
Pork and beef minced meat were contaminated with Cam- pylobacter at a very low level: on average, 2.5% and 0.6% in
25 g samples, respectively. Other studies at retail level have
shown a low prevalence of pork and beef meat (25 g samples).
In an Italian study (Zanetti et al., 1996), 2.4% of samples of
fresh pork sausages were found to be contaminated and a study
in the United States (Duffy et al., 2001), showed 1.6% positive
ground meat and sausage. Another Italian study revealed a 1.3%
prevalence in retail establishments (Pezzotti et al., 2003).
Between 2000 and 2003, the prevalence rates for Campylo-
bacter in all types of meat were statistically similar ( P N0.05),
except for chicken fillets and layer carcasses, which showed a
lower prevalence in 2001 to 2003 in comparison with 2000( P b0.05). These changes could be the result of the fact that the
surveillance plan, which started in 2000, had not been totally
optimal in that year.
4.4. Types of establishments and species of Campylobacter
sampled between 2000 and 2003
A comparison of the prevalence of Campylobacter between
production plants and retail establishments is shown in Fig. 2,
based on the cumulative 4-year results from 2000 to 2003. The
prevalence of broiler carcasses and fillets was significantly lower
at the retail establishments than at the production plants: 20.5%
and 12.1%, respectively, were positive for Campylobacter insupermarkets and butcheries. The lower rate of recovery of
Campylobacter at retail establishments is attributable to the
sensitivity of Campylobacter to desiccation, atmospheric air
and low temperature (Duffy et al., 2001). For layer carcasses,
the same prevalence was observed at production plants and
retail establishments, probably due to thawing at the retail
establishments.
More than 80% of the isolates from the poultry samples were
C. jejuni and 10–15% were C. coli. This was in accordance
with Belgian human data reported in 2003: 57.1% of the total
number of isolates of Campylobacter were C. jejuni, and 14.3%
were C. coli (Ducoffre, 2004). Other studies have also shown a predominance of C. jejuni in poultry samples: 67.8% of broiler
carcass isolates (Wilson, 2003), 69% of chicken isolates (Moore
et al., 2002) and 75% of skinless chicken breast isolates (Zanetti
et al., 1996).
Pork and beef minced meat had a slightly higher ( P N0.05)
prevalence at retail establishments in comparison with the
production plants. A similar observation was made regarding
raw pork meat at retail level by Pezzotti et al. (2003), who
explained this by the incidence of cross-contamination in
butcher's shops.
In pork and beef samples, 75% and 100% of isolates were
C. jejuni, respectively, as shown by other studies on the
intestinal content of cattle, but not of pork, where most of the
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Campylobacter have generally been found to be C. coli
(Anonymous, 2001; Pezzotti et al., 2003). This is in accordance
with the hypothesis of cross-contamination of pork minced meat
by poultry meat at the level of retail establishments, as observed
in the Italian study of Zanetti et al. (1996), where only C. jejuni
was found in pork sausage.
4.5. Campylobacter and the pork, beef and poultry processing
chains
Campylobacter have been frequently and consistently
isolated from poultry carcasses and meat of the following
reasons: no physical decontamination of the carcasses (such as
flaming or removal of the skin) has occurred, no chemical
decontamination mean is authorized in EU during the
slaughtering process, and the poultry skin remains moist, unlike
in the case of pork and beef carcasses. Cattle, pigs and poultry
are very frequently and highly contaminated by Campylobacter
in their intestinal tract: different authors have detected 53.9% of Campylobacter in cattle, 63.5% to 100% in pigs, and 82.9% in
broilers ( Nesbakken et al., 2003; Pearce et al., 2003; Pezzotti
et al., 2003). In pork and beef abattoirs, the respect for strict
slaughtering procedures, providing efficient scalding, singeing
or flaming and chilling, and ensuring the avoidance of faecal
contamination, limits dramatically the Campylobacter contam-
ination of meat (Borch et al., 1996).
At the poultry processing level, the use of measures that have
shown their efficiency for controlling Salmonella, such as
logistic slaughtering, are not very efficient in the control of
Campylobacter contamination (Rosenquist et al., 2003).
Cross-contamination between flocks occurs during transport
(by crates), slaughtering, especially during submerging andwashing in water, and during defeathering and eviscerating
(Berndtson et al., 1996). The cross-contamination occurs as a
result of significant contamination of the equipment and process
water on a slaughter line (Herman et al., 2003). Cutting, boning
and handling of poultry carcasses may also cause cross-
contamination, and Campylobacter can be found on carcasses,
fillets and prepared chicken meat at retail level, even on the
outer packaging of chickens (Humphrey et al., 2001; Jorgensen
et al., 2002). The prevalence of C. jejuni has been demonstrated
on surfaces in a processing environment and on cutting boards
(Cools et al., 2005b). Lowering the prevalence rate is difficult,
but could be achieved with Campylobacter -free flocks or decontamination immediately after slaughter and through
dressing by physical (removing the skin, heat treatment) or
chemical means (Corry and Atabay, 2001). Campylobacter are
more sensitive than most other vegetative bacteria to deconta-
minating agents, such as heat and irradiation, and this organism
cannot multiply in food or in the food processing environment.
However, poultry decontamination may be difficult to achieve
because some Campylobacter are trapped in or are attached to
the animal's skin (Corry and Atabay, 2001). The infective dose
of C. jejuni may be very low; it varies between 500 and 108
organisms (Oosterom et al., 1983a; Black et al., 1988; Hood
et al., 1988). In general, in the present study, the prevalence of
meat from retail establishments was lower than in samples from
production plants. This is probably due to the death of Cam-
pylobacter cells, but could also be due to the presence of some
viable but not cultivable forms of Campylobacter described
under certain stress conditions (Cools et al., 2005a).
In industrialized countries, 50–70% of all campylobacter-
iosis is attributable to the consumption of broiler chickens (Hu
and Kopecko, 2003; Keener et al., 2004). This has also beendemonstrated in Belgium, where a 40% decline in human
Campylobacter infections was observed in June 1999, during
the dioxin crisis, mainly because of the withdrawal of poultry
(Vellinga and Van Loock, 2002). In Belgium, some beef and
pork ground meat (and occasionally prepared chicken) is eaten
raw, which could constitute a health risk. Other causes of
campylobacteriosis, such as flies, could explain other cases and
the summer peak of campylobacteriosis in humans (Hald et al.,
2004; Ekdahl et al., 2005).
The high and unvarying contamination in the poultry primary
production sector makes necessary measures at this level in
addition to methods for minimizing cross-contamination. Fur-thermore, careful observation of hygiene rules while handling
and cooking products often containing Campylobacter (for
example, poultry, raw milk and untreated water, and also when
handling pets) is very important in the prevention of infection
(Allos, 2001). In order to choose the best risk management tools
and to establish adapted microbiological criteria for Campylo-
bacter , a quantitative microbiological risk assessment based on
quantitative data should be used (Anonymous, 2005a).
The European Food Safety Authority have recommended
controls that are mainly focused on live animals at the primary
production stage (Anonymous, 2005a). A survey plan in line
with the present study could be used in the future to follow the
effects of the planned measures and to follow the changes inCampylobacter contamination at all stages of the food chain
in the European Union.
Acknowledgements
The Belgian Federal Agency for the Safety of the Food
Chain gave financial support for this study. The authors also
acknowledge Marc Cornelis, Jean-Yves François, Martine
Jouret and François Ruttens for their work on the surveillance
plans and Frédéric Farnir for his support in statistics.
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