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Journal of Food Protection, Vol. 64, No. 1, 2001, Pages 1216


Copyright q, International Association for Food Protection

Salmonella in the Lairage of Pig Slaughterhouses


M. SWANENBURG, 1,2* H. A. P. URLINGS, 1,2 D. A. KEUZENKAMP, 1 AND J. M. A. SNIJDERS 1

1Department of the Science of Food of Animal Origin, Faculty of Veterinary Medicine, Utrecht University, P.O. Box 80.175, 3508 TD Utrecht,
The Netherlands; and 2Department of Food Science, Institute of Animal Science and Health, P.O. Box 65, 8200 AB Lelystad, The Netherlands

MS 00-76: Received 9 March 2000/Accepted 25 July 2000

ABSTRACT
The purpose of this study was to determine if lairages of pig slaughterhouses can act as a source of contamination of
slaughtered pigs with Salmonella. The prevalence and variety of serotypes of Salmonella in the lairages of two pig slaugh-
terhouses were determined, and the ef cacy of the usual cleaning and disinfection on the presence of Salmonella was estimated.
Lairages of two pig slaughterhouses were sampled three times when pigs were present. Furthermore, these lairages were
sampled after the usual cleaning and disinfection, whereas the lairage of one slaughterhouse was sampled an additional time
after improved cleaning and disinfection. Samples were collected by swabbing oor and wall surfaces and collecting the
residing uids on the oor throughout the lairage. Salmonella was isolated in 70 to 90% of the samples when pigs were
present. The usual cleaning and disinfection reduced the level of contamination with Salmonella to 25% positive samples,
whereas improved cleaning and disinfection reduced this level to 10% positive samples. It is concluded that the waiting period
in the lairage of at least 2 h contains a substantial risk for slaughter pigs to become infected with Salmonella, especially for
pigs originating from Salmonella-free herds. The usual cleaning and disinfection of the lairage were not suf cient to eliminate
this risk, whereas an improved procedure for cleaning and disinfection still was unsatisfactory.

Salmonella is an important cause of bacterial food- These experiments were carried out in the framework
borne infections. Each year approximately 450 per 100,000 of a research project on Salmonella in slaughter pigs in The
persons in The Netherlands suffer from salmonellosis, and Netherlands. The purpose of the study was to determine if
it is estimated that about 15% of these salmonellosis cases lairages of pig slaughterhouses can act as a source for con-
originate from pork (2). tamination with Salmonella of slaughtered pigs. Swab sam-
Pigs can become infected with Salmonella either di- ples and water samples were collected from the oors and
rectly via uptake of infected feed or contact with another walls of the lairages of two slaughterhouses at two time
infected pig or indirectly through a contaminated environ- points, when pigs were present and after cleaning and dis-
ment, such as surfaces, equipment, or persons. It is com- infection. We determined the prevalence of Salmonella in
monly thought that the lairage, where pigs are held from 2 all samples, after which the isolated Salmonella strains were
to 8 h before they are slaughtered, can act as an important genotyped by enterobacterial repetitive intergenic consen-
source of bacterial infections. However, only few studies sus polymerase chain reaction. Furthermore, in every sam-
have been carried out to determine the prevalence and the ple we estimated the total number of CFUs of aerobic bac-
variety of serotypes of Salmonella in pig lairages or to de- teria and Enterobacteriaceae.
termine the effect of cleaning and disinfection of the lairage
MATERIALS AND METHODS
on the prevalence of Salmonella. Weber (12) found 16 to
50% Salmonella-positive samples in lairages of German Lairages of two Dutch pig slaughterhouses (slaughterhouse
slaughterhouses after pigs had been in the lairage and 0 to 1 and 2), with a capacity of slaughtering 800 and 500 pigs per h,
33% Salmonella-positive samples after cleaning and disin- respectively, were each sampled three times during presence of
fection. Lazaro et al. (6) found 20% Salmonella-positive pigs (sampling days 1, 2, and 3) and one time after the usual
samples in the lairage of a pig slaughterhouse in Brazil. cleaning and disinfection (sampling day 4). The lairage of slaugh-
Since Fedorka-Cray et al. (5) and Blaha et al. (3) found terhouse 1 was sampled an additional time after improved clean-
that Salmonella can spread through the body of the pig very ing and disinfection (sampling day 5). Both lairages had basically
the same size and were constructed in the same way, which im-
rapidly after uptake, it would be reasonable to assume that
plied that logistic procedures were comparable. Floors and walls
pigs can easily become generally infected with Salmonella
of the lairages were made of concrete.
in the lairage of a slaughterhouse before slaughter. This has Slaughtering occurred from Monday to Friday. Cleaning and
already been shown by Williams and Newell (13), who disinfection were carried out on Saturdays in the usual way for
found the same Salmonella serotypes in the lairage before both slaughterhouses. Sampling during presence of pigs was car-
the pigs entered as in rectal and cecal swabs of the pigs ried out at three different days per slaughterhouse within a period
after their waiting period in the lairage. of 2 weeks, each day at the same time (in slaughterhouse 1: Tues-
day, rst week; Monday and Thursday, second week; in slaugh-
* Author for correspondence. Tel: 131 320 238176; Fax: 131 320 terhouse 2: Monday and Thursday, rst week; Tuesday, second
238961; E-mail: M.Swanenburg@id.wag-ur.nl. week). Sampling of the cleaned lairage was carried out on Sun-
J. Food Prot., Vol. 64, No. 1 SALMONELLA IN THE LAIRAGE OF PIG SLAUGHTERHOUSES 13

to the swab samples. Then the swabs were put in a stomacher for
2 min, after which they were squeezed out and removed from the
stomacher bag. Ten milliliters of concentrated buffered peptone wa-
ter was added to the water samples. Then the samples were gently
stirred. All samples were incubated at 378C for 18 to 24 h.
Selective enrichment Salmonella isolation procedure. The
pre-enrichment broth was mixed, and 0.1 ml was transferred to
9.9 ml of prewarmed Rappaport-Vassiliadis enrichment broth (Ox-
oid CM 669). This was incubated in a water bath of 428C for 24
to 48 h.
Selective and elective growth. A loop of material from the
Rappaport-Vassiliadis broth was transferred and spread onto the
surface of a brilliant green agar plate (Oxoid CM 329) so that
FIGURE 1. Schematic oor diagram of the sampled lairages. (A) isolated colonies could develop. The plates were incubated in in-
Entrance platforms, (B) corridor between entrance platforms and
verted position at 378C for 18 to 24 h. After incubation the plates
pens, (C) waiting pens, (D) corridor to restrainer, and () walk-
were checked for growth of typical Salmonella colonies (lightly
ing direction of pigs. transparent, reddish color). When no typical colonies were found
after 24 h of incubation, a loop of Rappaport-Vassiliadis (48 h
incubated) was plated out again on a brilliant green agar plate.
days (in slaughterhouse 1: 2 months after rst samplings; in
slaughterhouse 2: 3 weeks after rst sampling). In slaughterhouse Con rmation. When typical colonies had grown on the bril-
1, cleaning started with water to ush away the dirt. Thereafter, a liant green agar plate, up to 5 colonies per plate were transferred
cleaning solution (Kleencare CF6202, 5% active alkaline chloride and inoculated on triple sugar iron agar (Oxoid CM 277), which
combination) was used (contact time at least 1 h), which was was incubated at 378C for 18 to 24 h. When a positive reaction
washed away with water. Thereafter, the lairage was disinfected occurred after incubation (black color of agar, gas), bacterial ma-
with Kleencare DS6601 (5%, contains didecyldimethylammoni- terial from the triple sugar iron agar was agglutinated with poly-
umchloride), which also was washed away with water. The clean- valent Salmonella antiserum (Pro-lab Diagnostics, Neston, Wirral,
ing and disinfection solutions were approximately 308C. In UK). Isolated Salmonella strains were typed with monovalent spe-
slaughterhouse 2, cleaning was carried out with a lot of water. A ci c O antisera (Pro-lab Diagnostics) to identify O antigens.
cleaning or disinfection solution was not used. Both slaughter- The Salmonella strains were genotyped with a standardized
houses used potable water (high pressure) for cleaning. The im- enterobacterial repetitive intergenic consensus polymerase chain
proved cleaning in the lairage of slaughterhouse 1 was carried out reaction, rst described by Versalovic et al. (11) and amended by
in the same way as the normal cleaning and disinfection, but Swanenburg et al. (8). As described by Van Lith and Aarts (10)
additional to the normal procedures the cleaning was visually and Swanenburg et al. (8), genotypes could be related to serotypes
checked at the critical control points (drains, holes in the oor, (each serotype could be divided into one or more genotypes; each
rough surfaces of oor and wall, corners) by an experienced vet- genotype always had the same serotype). After genotyping, a rep-
erinary hygienist. Mistakes in cleaning were corrected, followed resentative number of strains was serotyped, according to the
by disinfection. Kauffmann-White scheme, at the Salmonella reference center
During the samplings in the presence of pigs, 25 swab sam- RIVM (National Institute of Public Health and the Environment)
ples and 20 water samples (residing uids on the oor: sprinkling at Bilthoven, The Netherlands. Serotyping was carried out with
water, feces, urine) were collected per sampling day, except for Salmonella antisera that were prepared at the Rijksinstituut voor
sampling day 1 at slaughterhouse 1 when 22 swab samples and Volksgezondheid en Milieuhygiene (RIVM).
19 water samples were collected. The swab method was described Furthermore, to measure the hygienic status of the lairage,
by Van den Elzen and Snijders (9). Per sample a surface of 50 by the total numbers of CFUs of aerobic bacteria and Enterobacte-
50 cm was swabbed with both sides of the swab. Water samples riaceae (per cm2 or ml) were determined by diluting the samples
of 100 ml were collected with a sterile pipette. Samples were and growing them on plate count agar, which was incubated 3
collected throughout the whole lairage at the following locations: days at 308C, and violet red bile glucose agar (poured plates,
the oor of the entrance platforms, the wall of the entrance plat- Oxoid CM 485), which was incubated 24 h at 378C. The statistical
forms, the oor of the corridor between entrance platforms and detection level (the lowest number of Enterobacteriaceae that
pens, the oor of the pens, and the oor of the corridor leading could possibly be detected: at least 1 colony on plate) was 21.4
to the restrainer. Figure 1 shows a oor diagram of the lairages in log CFU/cm2 for the swab samples and 20.05 in log CFU/ml
to indicate sampling locations. for the water samples.
The results were evaluated statistically by the chi-square test
During the samplings after cleaning and disinfection, water
(comparison of numbers of Salmonella-positive samples) and by
samples could not always be collected, because there was not
an independent samples t test (two groups) or one-way analysis
enough water present on the oors. Therefore, a different number
of variance (more than two groups), followed by a least signi cant
of samples was collected: 40 swabs and 10 water samples on
difference test, when signi cance was established (comparison of
sampling day 4 in slaughterhouse 1 and 50 swabs on sampling
numbers of total CFUs of aerobic bacteria and Enterobacteri-
day 5 in slaughterhouse 1 and on sampling day 4 in slaughter-
acea), using SPSS software, version 7.0 (1). Signi cance was de-
house 2. After sampling, all samples were transported to the lab-
termined with P , 0.05.
oratory at a temperature of 48C. Salmonella isolation procedures
started 1 to 2 h after sampling. RESULTS
Pre-enrichment Salmonella isolation procedure. Fifty mil- Salmonella could be isolated from all locations of the
liliters of buffered peptone water (with 0.1% Tween 80) was added lairages in both slaughterhouses when pigs were present.
14 SWANENBURG ET AL. J. Food Prot., Vol. 64, No. 1

CFUs of aerobic bacteria in the water samples differed sig-


ni cantly between sampling day 2 (7.54 6 0.47) and 3
(7.08 6 0.48) in slaughterhouse 1 (P 5 0.002) and between
sampling day 1 (7.37 6 0.44) and 2 (7.72 6 0.47) in
slaughterhouse 2 (P 5 0.017).
After normal cleaning and disinfection (only cleaning
in slaughterhouse 2), the lairages still contained rests of
feces, especially around the water outlets. Also some rest
water of cleaning and disinfection was present on the oor
of both lairages. The results showed that neither cleaning
alone nor cleaning followed by disinfection was able to
eliminate all Salmonella, although the percentage of Sal-
FIGURE 2. Percentages of Salmonella-positive swab and water
samples in the lairages of two pig slaughterhouses. Days 1, 2, monella-positive samples in the lairages of both slaughter-
and 3: during presence of pigs. Day 4: after usual cleaning (and houses was signi cantly decreased. Salmonella was isolated
disinfection). Day 5: after improved cleaning and disinfection. Sl. from 25% of the swab samples and none of the water sam-
1, slaughterhouse 1; Sl. 2, slaughterhouse 2. ples of slaughterhouse 1 and 24% of the swab samples of
slaughterhouse 2. This implies that the lairages still were
Figure 2 shows the percentages of Salmonella-positive highly contaminated with Salmonella. After improved
swab and water samples on each sampling day in both cleaning and disinfection of the lairage at slaughterhouse 1,
slaughterhouses. Salmonella was isolated from 89% of the Salmonella was isolated from 10% of the swab samples.
swab samples and 95% of the water samples (mean per- This result showed that it was possible to clean the lairage
centage of 3 sampling days) when pigs were present in better than is usually done but that it will be dif cult to
slaughterhouse 1, whereas Salmonella was isolated from eliminate all salmonellae from the lairage.
79% of the swab samples and 62% of the water samples After cleaning and disinfection, numbers of CFUs of
when pigs were present in slaughterhouse 2. The number aerobic bacteria and Enterobacteriaceae were signi cantly
of Salmonella-positive samples was not signi cantly in u- reduced (P , 0.05) in the lairages of both slaughterhouses
enced by sampling day or slaughterhouse, except for sam- (Table 1). After improved cleaning and disinfection in
pling day 1 at slaughterhouse 2, when the number of Sal- slaughterhouse 1, the number of Enterobacteriaceae was
monella-positive samples was signi cantly lower (P , lower than after normal cleaning and disinfection (P 5
0.05) than on the other sampling days. The number of Sal- 0.051).
monella-positive samples was also not signi cantly in u- Genotyping of Salmonella isolates resulted in 13 dif-
enced by the kind of sample collected (swab or water sam- ferent genotypes isolated from the lairage of slaughterhouse
ple). 1 and 10 different genotypes isolated from the lairage of
In both slaughterhouses, the numbers of CFUs of aer- slaughterhouse 2. In total, 16 different genotypes were iso-
obic bacteria were around 6 in log units per cm2 and num- lated. Table 2 shows the different genotypes and corre-
bers of CFUs of Enterobacteriaceae were around 3 to 4 in sponding serotypes that were isolated in both slaughter-
log units per cm2 (Table 1) when pigs were present. Slaugh- houses. The most common serotype in the lairage of
terhouse and sampling day had no signi cant effect on the slaughterhouse 1 during the presence of pigs was Salmo-
number of CFUs of Enterobacteriaceae in either swabs or nella Panama, which was not isolated after cleaning any-
water samples, but the number of CFUs of aerobic bacteria more. Another common serotype, isolated each sampling
in both swab and water samples was signi cantly higher in day in this slaughterhouse, was Salmonella Typhimurium.
slaughterhouse 2 (P 5 0.009). The mean 6 SD number of The most common serotype in the lairage of slaughterhouse

TABLE 1. Average numbers of colony-forming units of aerobic bacteria and Enterobacteriaceae in swabs and water samples collected
in the lairages of two pig slaughterhouses
Log CFU/cm2 Log CFU/cm2
or ml of or ml of
Slaughter- Sampling No. of aerobic bacteria Enterobacteriaceae
house Situation technique samples 6 SD 6 SD

1 Pigs present Swabs 72 5.7 6 0.9 3.5 6 1.2


Water 59 7.3 6 0.5 5.0 6 0.6
After cleaning Swabs 40 3.1 6 1.4 20.4 6 1.6
Water 10 2.1 6 1.1 0.0 6 0.2
After improved Swabs 50 Not done 20.7 6 1.2
cleaning
2 Pigs present Swabs 75 6.0 6 0.5 3.6 6 0.8
Water 60 7.5 6 0.5 5.1 6 0.6
After cleaning Swabs 50 4.5 6 0.9 20.1 6 1.5
J. Food Prot., Vol. 64, No. 1 SALMONELLA IN THE LAIRAGE OF PIG SLAUGHTERHOUSES 15

TABLE 2. Genotypes and corresponding serotypes of Salmonella in two pig slaughterhousesa


Distribution of Salmonella genotypes in contaminated samples (%)b

Slaughterhouse 1 Slaughterhouse 2

Genotype/serotype D1 D2 D3 D4 D5 D1 D2 D3 D4

B-A/Typhimurium 39 40 31 90 50 95 77 80 83
B-C/Derby 3 17 12 17
B-E/Typhimurium 3
B-G/Brandenburg 3 3 24 20
B-J/Bredeney 5
B-L/Brandenburg 10 20
B-S/Senftenberg 8
C-A/Infantis 18 10 20 10
C-B/Livingstone 3 15 2 11
C-C/Bovismorbi cans 8
C-G/Goldcoast 20
C-F/Mbandaka 7 5
D-A/Panama 68 58 60 9
E-A/Give 29
E-B/London 11 7 10 10 8
E-E/Elisabethville 29
No. of positive samples 38/41 40/45 42/45 10/50 5/50 20/45 35/45 41/45 12/50
a Days 1, 2, and 3: during presence of pigs. Day 4: after usual cleaning (and disinfection). Day 5: after improved cleaning and disinfection.
b The total of one day can be more than 100% due to the presence of several genotypes in a single sample.

2, as well as in the presence of pigs after cleaning, was (12) concluded that more Salmonella could be isolated from
Salmonella Typhimurium. Seven genotypes were isolated pigs that were kept in lairage for a waiting period of 18 to
from lairages of both slaughterhouses, whereas six geno- 20 h compared with pigs that were slaughtered directly after
types were exclusively isolated from the lairage of slaugh- arrival at the slaughterhouse. In contrast, Craven and Hurst
terhouse 1 and three genotypes were exclusively isolated (4) concluded that fewer pigs had Salmonella in the ceca
from the lairage of slaughterhouse 2. after 2 or 3 days in lairage.
The results of our experiments strongly suggest that the
DISCUSSION
lairage, as a result of the high level of contamination with
These experiments show that almost the whole lairage Salmonella, can have a signi cant effect on the number of
was contaminated with several strains of Salmonella when Salmonella-infected pigs at slaughter. Exploring the envi-
pigs were present. Salmonella could be isolated from al- ronment is part of the normal behavior pattern of pigs. This
most every sample collected in the lairages of the two exploring behavior consists of snif ng, rooting, and drink-
slaughterhouses, and up to eight different serotypes could ing, which offers a great possibility for the pigs to infect
be isolated per sampling day. Numbers of CFUs of aerobic themselves with Salmonella, after which the infection can
bacteria were around 6 log units per cm2, and numbers of spread rapidly through the whole pig. This suggestion is
CFUs of Enterobacteriaceae were around 3 to 4 log units supported by the results of the study by Fedorka-Cray et
per cm2 . On sampling day 1 at slaughterhouse 2, Salmo- al. (5), who concluded from their experiments that Salmo-
nella was isolated from signi cantly fewer samples than on nella Typhimurium could be detected from tonsil, cecum,
the other sampling days in both slaughterhouses. We do not colon, and thoracic tissues 3 h after intranasally inoculation
have an explanation for this observation. of pigs, and by the results of the study by Blaha et al. (3),
Only a few studies have been conducted on the Sal- who concluded that orally given Salmonella Typhimurium
monella contamination of a lairage. Weber (12) found 16 could be detected in ileocecal lymph nodes 4 h after Sal-
to 50% Salmonella-positive swab samples in lairages of monella was administered to the pigs and in tonsils already
German slaughterhouses after pigs had been in and 0 to 30 min after administration.
33% Salmonella-positive swab samples after cleaning and Furthermore, this study shows that the normal
disinfection. Lazaro et al. (6) found 20% Salmonella-posi- cleaning and disinfection procedures of the lairages are un-
tive swab samples in the lairage of a pig slaughterhouse in able to eliminate Salmonella. Twenty- ve percent of the
Brazil. Furthermore, experiments have been done in which swab samples still contained Salmonella after cleaning and
the effect of the waiting time in the lairage on the number disinfection, indicating a relatively high level of contami-
of pigs infected with Salmonella was tested (4, 7, 12), but nation. This is supported by the fact that still three (slaugh-
the conclusions of these experiments were not consistent. terhouse 1) or four (slaughterhouse 2) different serotypes
Morgan et al. (7) concluded that the number of pigs car- were isolated after cleaning and disinfection. Moreover,
rying Salmonella in the ceca increased signi cantly in pigs even improved cleaning and disinfection were not suf cient
held for extended periods (2 or 3 days) in lairage. Weber to eliminate all Salmonella, although the number of positive
16 SWANENBURG ET AL. J. Food Prot., Vol. 64, No. 1

samples decreased. The main factor that causes the dif - icting interests concerning animal welfare (rough oors)
culty in cleaning and disinfection of the lairage is the way and hygiene (smooth oors) are a basic dilemma to improve
it is constructed. The oor and wall surfaces are very un- this situation.
even and contain many small and bigger holes. Cleaning ACKNOWLEDGMENTS
and disinfection solutions penetrate badly in these holes.
We thank the Dutch Product Boards for Livestock, Meat and Eggs
Furthermore, water and rests of feces can easily stay behind
for nancing the project. We also thank the staff and personnel of the two
in the holes after the cleaning and disinfection solutions are slaughterhouses for their willingness to participate in the study and their
washed away, which is one of the reasons why even im- cooperation during the experiments.
proved cleaning and disinfection were not able to eliminate
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