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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 campylobacteriosis 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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