Cross contamination of turkey carcasses by Salmonella species during defeathering.
ABSTRACT Salmonella present on the feathers of live birds could be a source of contamination to carcass skin during defeathering. In this study, the possibility of transfer of Salmonella from the feathers of live turkeys to carcass tissue during the defeathering process at a commercial turkey processing plant was investigated. The contribution of scald water and the fingers of the picker machines to cross contamination were also examined. Over 4 visits, swab samples were collected from 174 randomly selected tagged birds before and after defeathering. Two swab samples from the fingers of the picker machines and a sample of scald water were also collected during each visit. Detection of Salmonella was carried out following standard cultural and identification methods. The DNA fingerprints obtained from pulsed field gel electrophoresis of Salmonella serotypes isolated before and after defeathering, from scald water, and from the fingers of the picker machines were compared to trace cross contamination routes. Salmonella prevalence was similar before and after defeathering during visits 2 and 3 and significantly increased after defeathering during visits 1 and 4. Over the 4 visits, all Salmonella subtypes obtained after defeathering were also isolated before defeathering. The results of this study suggest that Salmonella was transferred from the feathers to carcass skin during each visit. On each visit, the Salmonella subtypes isolated from the fingers of the picker machines were similar to subtypes isolated before and after defeathering, indicating that the fingers facilitate carcass cross contamination during defeathering. Salmonella isolated from scald water during visit 4 was related to isolates obtained before and after defeathering, suggesting that scald water is also a vehicle for cross contamination during defeathering. By using molecular subtyping, this study demonstrated the relationship between Salmonella present on the feathers of live turkeys and carcass skin after defeathering, suggesting that decontamination procedures applied to the external surfaces of live turkeys could reduce Salmonella cross contamination during defeathering.
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ABSTRACT: Salmonella Schwarzengrund is one of the causative agents of human salmonellosis and animal infections. High prevalence of multidrug resistant strains of S. Schwarzengrund from chicken meat has been recently reported in Taiwan. With an attempt to see if such prevalence in chicken meat was due to the recirculation of S. Schwarzengrund strains in traditional marketplaces, a total of 173 S. Schwarzengrund strains isolated between 2000 and 2005 from 417 retail chicken meat samples purchased from Taipei, Taiwan were analyzed using pulsed field gel electrophoresis (PFGE) method. For XbaI and AvrII digested DNA, a total of 23 and 16 PFGE patterns, respectively, were obtained. When these patterns were combined, a total of 47 subtypes were obtained and the major subtypes were X3A2, X1A2 and X2A1. Since it was found that these major subtypes were repeatedly found for multidrug resistant strains collected from 2000 to 2005, we then collected the chicken meat isolates from central and southern Taiwan in 2006. These strains did not show similar major subtypes as those found in Taipei. Such results might also suggest that the repeated appearance of some major subtypes for S. Schwarzengrund strains isolated each year in Taipei was due to the recirculation of these strains in retail marketplace during these years.Food Microbiology 05/2011; 28(3):399-405. · 3.41 Impact Factor
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ABSTRACT: Fitness benefits associated with the development of a costly immune system would include not only self-protection against pathogenic microorganisms but also protection of host offspring if it reduces the probability and the rate of vertical transmission of microorganisms. This possibility predicts a negative relationship between probabilities of vertical transmission of symbionts and level of immune response that we here explore inter-specifically. We estimated eggshell bacterial loads by culturing heterotrophic bacteria, Enterococcus, Staphylococcus and Enterobacteriaceae on the eggshells of 29 species of birds as a proxy of vertical transmission of bacteria from mother to offspring. For this pool of species, we also estimated innate immune response (natural antibody and complement (lysis)) of adults, which constitute the main defence against bacterial infection. Multivariate general linear models revealed the predicted negative association between natural antibodies and density of bacteria on the eggshell of 19 species of birds for which we sampled the eggs in more than one nest. Univariate analyses revealed significant associations for heterotrophic bacteria and for Enterobacteriaceae, a group of bacteria that includes important pathogens of avian embryos. Therefore, these results suggest a possible trans-generational benefit of developing a strong immune system by reducing vertical transmission of pathogens.Naturwissenschaften 09/2011; 98(9):807-13. · 2.14 Impact Factor
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ABSTRACT: The aim of the study was to find out the serotype distribution of 169 Salmonella colonies recovered from 112 Salmonella positive ground turkey (115 colonies) and 52 turkey meat parts (54 colonies). Out of 15 Salmonella serotypes: S. Corvallis, S. Kentucky, S. Bredeney, S. Virchow, S. Saintpaul and S. Agona were identified as the predominant serovars at the rates of 27%, 13%, 12%, 12%, 11%, and 10%, respectively. Other serotypes were below 6% of the total isolates. All S. Kentucky and S. Virchow and most of the S. Corvallis (39/46) and S. Heidelberg (9/9) serotypes were recovered from ground turkey. The results indicate that turkey ground meat and meat parts were contaminated with quite distinct Salmonella serotypes. This is the first study reporting Salmonella serotype distribution in turkey meat and S. Corvallis as predominant serotype in poultry meat in Turkey.BioMed research international. 01/2013; 2013:281591.
Cross Contamination of Turkey Carcasses by Salmonella
Species During Defeathering1
C. W. Nde, J. M. McEvoy, J. S. Sherwood, and C. M. Logue2
The Great Plains Institute of Food Safety, Department of Veterinary and Microbiological Sciences,
North Dakota State University, Fargo 58105
birds could be a source of contamination to carcass skin
tissue during the defeathering process at a commercial
turkey processing plant was investigated. The contribu-
tion of scald water and the fingers of the picker machines
to cross contamination were also examined. Over 4 visits,
swab samples were collected from 174 randomly selected
tagged birds before and after defeathering. Two swab
samples from the fingers of the picker machines and a
sample of scald water were also collected during each
visit. Detection of Salmonella was carried out following
standard cultural and identification methods. The DNA
fingerprints obtained from pulsed field gel electrophore-
sis of Salmonella serotypes isolated before and after de-
feathering, from scald water, and from the fingers of the
tion routes. Salmonella prevalence was similar before and
after defeathering during visits 2 and 3 and significantly
Salmonella present on the feathers of live
Key words: Salmonella, turkey, defeathering, cross contamination
2007 Poultry Science 86:162–167
Salmonella is one of the leading causes of bacterial
foodborne illness in the United States, with an annual
economic impact estimated at $0.5 to 2.3 billion (Frenzen
et al., 1999). Poultry meat is commonly implicated in
ers and turkeys reported as vehicles. Identifying sources
of contamination during slaughter and processing and
implementing strategies to reduce, eliminate, or prevent
such contamination are key to reducing the prevalence
of Salmonella on poultry and the consequent incidence of
2007 Poultry Science Association Inc.
Received May 10, 2006.
Accepted September 30, 2006.
1Acknowledgement of grant: USDA CSREES Special Research Grant
#TE2003-06068. Apreliminaryreportof thisstudywaspublished inthe
proceedings of the Conference of Research Workers in Animal Disease,
Chicago, IL, November 2004.
2Corresponding author: Catherine.Logue@ndsu.edu
increased after defeathering during visits 1 and 4. Over
the 4 visits, all Salmonella subtypes obtained after de-
feathering were also isolated before defeathering. The
results of this study suggest that Salmonella was trans-
ferred from the feathers to carcass skin during each visit.
On each visit, the Salmonella subtypes isolated from the
fingers of the picker machines were similar to subtypes
isolated before and after defeathering, indicating that the
fingers facilitate carcass cross contamination during de-
feathering. Salmonella isolated from scald water during
visit 4 was related to isolates obtained before and after
defeathering, suggesting that scald water is also a vehicle
for cross contamination during defeathering. By using
molecular subtyping, this study demonstrated the rela-
tionship between Salmonella present on the feathers of
live turkeys and carcass skin after defeathering, sug-
gesting that decontamination procedures applied to the
external surfaces of live turkeys could reduce Salmonella
cross contamination during defeathering.
human salmonellosis. To date, most studies of Salmonella
crosscontamination duringpoultry processinghave used
broilers, and there is limited information relating to
Birds presented for processing may harbor Salmonella
in their feces but not show any symptoms of disease
(Rigby and Petit, 1980, 1981; Higgins et al., 1982) and
serve as potential contamination sources to uncontami-
Defeathering, evisceration, and chilling are processing
stages where cross contamination may occur (James et
al., 1992; Hafez et al., 1997; Ono and Yamamoto, 1999).
Contaminated external surfaces such as feathers may
have a direct contaminating effect on carcass skin during
early processing stages, but there are few data document-
ing this effect. To date, no study has examined the rela-
of live birds and defeathered carcasses.
The defeathering process, which consists of scalding,
followed by mechanical feather removal, has been re-
ported to be a site of significant microbial cross contami-
SALMONELLA CROSS CONTAMINATION DURING TURKEY DEFEATHERING
nation (Ono and Yamamoto, 1999). Possible mechanisms
of bacterial cross contamination during defeathering in-
clude aerosols (Allen et al., 2003a,b), direct contact be-
tween contaminated and uncontaminated carcasses
(Mulder et al., 1978), and the action of the fingers of the
picker machines (Clouser et al., 1995a,b; Berrang et al.,
2001; Allen et al., 2003a,b). Studies of cross contamination
lence that occurs before and after defeathering and the
dissemination pattern of an indicator organism from an
artificially contaminated bird to other birds during pro-
cessing (Clouser et al., 1995a,b; Allen et al., 2003a,b). To
our knowledge, no study has examined the relationship
between Salmonella subtypes isolated before and after de-
Molecular typing is increasingly being used to comple-
ment conventional methodologies to elucidate bacterial
transmission routes (De Cesare et al., 2001; Sander et
al., 2001). Several studies have used molecular typing to
understand the transmission of Salmonella within poultry
production (De Cesare et al., 2001; Bailey et al., 2002;
Liebana et al., 2002; Crespo et al., 2004). The application
of such techniques will provide a better understanding
of the mechanisms of cross contamination that may occur
In this study, the breast feathers of turkeys were sam-
pled before defeathering and the exposed breast skin of
carcasses after defeathering to determine the extent of
cross contamination occurring during defeathering. Sero-
typing and pulsed field gel electrophoresis (PFGE) were
used to more specifically determine the relationship be-
tween Salmonella isolates obtained pre- and postde-
MATERIALS AND METHODS
Description of the Defeathering System
This study was carried out in a commercial turkey
processing plant that processes live turkeys to raw and
cooked finished products. Turkeys were processed at an
average speed of 800 carcasses/h. Birds were stunned,
a 20 to 30 ft tunnel. Carcasses were immersed in a scald
tank that was continuously supplied with steam-heated
water pumped through pipes at the bottom of the tanks.
Samples were collected on each of 4 visits to the plant
that were planned to coincide with the slaughter of flocks
from farms with a history of Salmonella contamination.
The temperature of scald tank water on the first 2 study
visits. The average immersion time per bird in the scald
tank was 2.2 min. After scalding, the carcasses were con-
veyed to the picker machines, which consisted of 2 com-
partments. The first compartment was a Barker Gent-L-
Flex picker with hock and straddle picker add-ons
removes about 90% of all feathers. The second compart-
ment was a Dura II-T (Simon Johnson, Barker/Foodcraft)
picker, which removes the remaining feathers. The total
time for feather removal for each carcass was about 2.2
min, bringing the total defeathering time to 4.4 min.
To ensure that the same randomly selected birds were
sampled before and after the defeathering process during
each visit, brightly colored plastic zip-ties were inter-
locked on the metal link above the shackles holding the
selected live birds. After the tagged carcasses emerged
from the picker machine, a second set of samples was
collected. Over 4 visits, 174 samples were collected at
predefeathering and 174 samples were collected at post-
defeathering. Two swab samples were collected from the
fingers of the picker machines, and 1 sample of scald
water was collected during each visit.
Commercially available sponges (Whirl-Pak Speci-
Sponge, Nasco, Fort Atkinson, WI) moistened with 10-
mL single strength buffered peptone water (BPW; Oxoid
Ltd., Basingstoke, UK) were used for carcass and picker
ile gloved hand, the sponge was squeezed inside the bag
to remove excess liquid before using it to swab an unde-
limited 100 cm2area on the breast feathers of randomly
selected tagged live birds. Following defeathering, an un-
delimited 100 cm2area of the carcass breast tissue of the
tagged defeathered bird was swabbed. Swabbing before
and after defeathering was carried out 10 times vertically
and 10 times horizontally using opposite sides of the
sponges. For picker finger sampling, sponges were han-
dled in the same manner as with carcass sampling and
were used to swab an undelimited 200 cm2area of the
picker machines that included the rubber fingers. After
sampling, all swabs were returned to their original bags.
Thirty milliliters of scald water was collected using a
sterile water “dippa” sampler with an integral handle
(Bibby Sterilin, Staffordshire, UK). All swab and scald
water samples were stored in a chilled container and
transported to the laboratory within 2 h of sample col-
Forty milliliters of single strength BPW (Oxoid) was
added to sponge samples and stomached for 90 s. For
scald water samples, a 15-mL aliquot was added to 15
mL of double strength BPW (Oxoid). Sponge and scald
water samples were incubated at 37°C for 18 to 24 h.
Following incubation, aliquots of 0.5 and 0.1 mL of the
BPW enriched samples were transferred to 10 mL of Tet-
rathionate (Difco, Sparks, MD) and 10 mL of Rappaport
Vassiliadis broth (Difco) and incubated at 42°C for 18 to
24 h. After incubation, a loopful of Tetrathionate and
Rappaport Vassiliadis broth were streaked onto XLT4
NDE ET AL.
Table 1. Prevalence of Salmonella-positive birds at pre- and postde-
no. positive birds/
no. sampled (%)
no. positive birds/
no. sampled (%)
a,bPercentages within a row lacking a common superscript differ (P
Salmonella colonies, when available, were picked from the
selective agar plates and streaked onto Lysine Iron Agar
(Difco) andTriple Sugar Iron(Difco) agar slantsand incu-
bated at 37°C for 18 to 24 h. Suspect Salmonella colonies
following biochemical screening were confirmed using
the Sensititre method for automated identification of
gram-negative organisms (AP 80, Trek Diagnostics,
Cleveland, OH). Confirmed Salmonella isolates were sero-
typed by the National Veterinary Services Laboratories,
Pulsed Field Gel Electrophoresis
of Salmonella Isolates
Identified Salmonella isolates were subtyped by PFGE
using the standardized protocol described by the Centers
for Disease Control and Prevention National Molecular
Subtyping network for Foodborne Disease Surveillance
(CDC, 2001). Salmonella Branderup H9812 (ATCC#: BAA-
664) was used as the reference strain.
The DNA macrorestriction fragments were resolved on
1% SeaKem Gold Agarose (Cambrex Bio Science Rock-
land Inc., Rockland, ME) in 0.5× Tris-borate EDTA. Then
PFGE was carried out in 0.5× Tris-borate EDTA using the
Chef Mapper PFGE system (BioRad, Hercules, CA) with
recirculation at 14°C. Run time for electrophoresis was
18 h with initial switch time of 2.16 s and final switch time
of 63.8 s. Following electrophoresis, gels were stained in
ethidium bromide for 30 min. Destaining was carried out
tion patterns on agarose gels were captured using an
imager (Alpha Innotech UV imager, San Leandro, CA)
and stored as .tif files. Macrorestriction patterns were
compared using the BioNumerics Fingerprinting II In-
formatrix software (Version 3.0, Applied Maths, Austin,
lated using the Dice correlation coefficient option of the
software with a position tolerance of 1% and an optimiza-
tion of 5%. The unweighted-pair group method using
average linkages (UPGMA; Struelens, 1996) was used to
construct dendrograms. A 70% similarity index was used
to distinguish different clusters on the dendrograms.
The McNemars test was performed using SAS 9 (SAS
Institute Inc., 2004) to determine if there was a significant
change in the prevalence of Salmonella-positive birds after
defeathering for each visit. The McNemars test was also
used to determine if there was a difference between the
overall Salmonella prevalence before and after defeathe-
ring when all 4 visits were combined (Table 1).
Change in the Prevalence of Salmonella-
Positive Birds at Pre- and Postdefeathering
During visits 1 and 4, the Salmonella prevalence after
defeathering was significantly higher (P < 0.05) than be-
fore defeathering (Table 1). There was no significant dif-
ference in Salmonella prevalence pre- and postdefeath-
ering during visits 2 and 3. When all 4 visits were com-
bined, there was an overall significant increase (P < 0.05)
in Salmonella prevalence after defeathering.
Dendrogram analysis revealed 4 clusters each for visits
1, 2, and 3, as well as 5 clusters for visit 4 (results not
shown). During all visits,serotyping correlated with clus-
tering because only identical serotypes were in the same
cluster. Using visit 3 as an example, Figure 1 shows the
dendrogram generated. Clusters 1 and 2 contain only
S. Hadar isolates, whereas clusters 3 and 4 contain S.
Relationship Among Salmonella Subtypes
Isolated at Pre- and Postdefeathering,
from Scald Water and the Rubber
Fingers of the Picker Machines
All Salmonella serotypes isolated after defeathering
were also isolated before defeathering (Table 2). Salmo-
nella serotypes with similar PFGE profiles were detected
at pre- and postdefeathering and on the fingers of the
picker machines during all 4 visits (Table 2). During visits
1 and 3, S. Hadar was isolated at the pre- and postde-
feathering stages and on the fingers of the picker ma-
chines (Table 2). During visit 2, S. Schwarzengrund was
of the picker machines (Table 2). During visit 4, S. Hadar
was detected in scald water at pre- and postdefeathering
and from the fingers of the picker machines (Table 2).
The results of this study showed that there was transfer
of Salmonella from live turkeys to carcass skin during
defeathering. Cross contamination during defeathering
SALMONELLA CROSS CONTAMINATION DURING TURKEY DEFEATHERING
Figure 1. Dendrogram showing pulsed field gel electrophoresis (PFGE) profiles of Salmonella isolates from visit 2. Pre = Predefeathering; Post =
postdefeathering; Fingers = fingers of picker machines.
NDE ET AL.
Table 2. Salmonella serotypes detected before and after defeathering, in
scald water, and on the picker fingers during each visit1
1Pre = predefeathering; Post = postdefeathering; PFGE = pulsed field
resulted in at least a similar number of birds being con-
taminated after defeathering as before (visits 2 and 3).
On the other 2 occasions, there was a significant increase
(P < 0.05) in the Salmonella prevalence after defeathering.
This is in agreement with previously reported data from
chicken and turkey carcass defeathering operations (Lil-
lard, 1989, 1990; Clouser et al., 1995a,b) where Salmonella
contamination after defeathering was observed to in-
crease or remain the same.
facilitated the determination of the source and transmis-
sion route of Salmonella contamination during defeath-
ering. This is in contrast to previous studies of cross con-
tamination during defeathering where conclusions were
limited by a lack of subtyping data.
This is the first report of a clear link between Salmonella
contamination of turkey feathers and subsequent carcass
contamination.Previous studieshave determinedthe Sal-
monella status of live birds by sampling feces (Rigby and
Petit, 1980, 1981; Higgins et al., 1982). In another study,
the increase in Campylobacter contamination of broilers
that occurred after defeathering was attributed to the
of the fingers of the picker machines (Berrang et al., 2001).
The results of the current study indicate that contami-
nated feathers should also be considered as a source of
carcass contamination. Given that such contamination is
on the external surface of bird, it is reasonable to suggest
that it could be a more significant source of carcass con-
tamination than feces that is normally internal.
The detection of the same Salmonella subtype in scald
water and at pre- and postdefeathering during visit 4
indicates that scald water is a vehicle for the transfer of
Salmonella between birds. This is supported by another
study in which Escherichia coli K12 was used as an indica-
tor organism to demonstrate cross contamination during
scalding (Mead et al., 1994). Despite the difference in the
scalding temperature between visits 1 and 2 (60°C) and
visits 3 and 4 (63.5°C), it is unlikely that Salmonella was
absent in scald water during visit 1 and 2. Salmonella has
previously been isolated from scald water at 60°C (Nivas
et al., 1973). Collecting 1 sample of scald water per visit
during the current study may have been a limiting factor
for Salmonella detection. Parameters such as sample vol-
umes, sample numbers, and culturing procedures may
also influence Salmonella detection in scald water (Cason
et al., 2000). Further studies that incorporate these vari-
ables will provide more information on the potential of
scald water as a vehicle for cross contamination during
The isolation of similar Salmonella subtypes from the
fingers of the picker machines during all 4 visits (Table
2) and from birds at pre- and postdefeathering supports
the role of the picker fingers in carcass cross contamina-
tion. This is in agreement with previous studies that have
reported thatthe fingers ofpicker machinesmay facilitate
bacterial cross contamination between carcasses (Clouser
et al., 1995b; Berrang et al., 2001).
Neither scald water nor the fingers of the picker ma-
chines are cleaned nor replaced between carcasses, sup-
porting their potentialfor facilitating cross contamination
between Salmonella-contaminated birds and Salmonella-
negative birds when they are processed in succession.
Scald water and the fingers of the picker machines may
also contribute to the contamination of Salmonella-free
flocks when they are processed following a Salmonella-
The results of this study show evidence for the possible
transfer of Salmonella from turkey feathers to carcass skin
during defeathering. This direct contaminating effect was
greater during visits 1 and 4 when the Salmonella preva-
contamination on the turkeys feathers may, therefore, be
a useful indicator of the potential for cross contamination
during defeathering. Future strategies could focus on re-
ducing the level of Salmonella on the feathers of live birds,
thus minimizing the risk of cross contamination during
The authors gratefully acknowledge John Reber and
Qiongzhen Li of North Dakota State University for statis-
tical analysis and technical assistance during sample col-
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