Split Marketing as a Risk Factor for Salmonella enterica
Infection in Swine
Marcos H. Rostagno,1H. Scott Hurd,2and James D. McKean2
On-farm reduction of Salmonella carriage prevalence in pigs requires the identification of risk factors to direct
interventions development. This study was designed to determine if split marketing of finishing pigs constitutes
a risk factor for Salmonella infections, by comparing Salmonella prevalence in the first group of pigs selected for
harvest (‘‘first pull’’) versus the prevalence in the last group of pigs selected for harvest (‘‘close out’’) from
multiple commercial finishing lots. Nine paired samplings were conducted consisting in matched groups of pigs
from individual barns as the first pull and the close out with a 4-week interval between groups. From each
group, fecal and meat samples were collected, on-farm and at harvest, respectively. Fecal samples were selec-
tively enriched, and analyzed for the presence of Salmonella, whereas meat juice samples were analyzed for the
presence of antibodies against Salmonella. In 7=9 (77.8%) of the studied barns, an increase in Salmonella preva-
lence was observed, based on both bacteriologic and serologic analysis. Overall, there was an increase of 9.2%
(p<0.05) in bacteriologic prevalence, and 31.3% (p<0.05) in serologic prevalence from first pull to close out
groups. This study demonstrates that a significant increase in Salmonella prevalence occurs between the first and
the last group of pigs harvested from finishing lots, with close out groups of market pigs posing a higher risk for
a potential risk for contamination of pork products. In the
United States, more than 76 million cases of foodborne illness
occur annually, and more than 95% of all cases of salmonel-
losis in humans are attributed to contaminated food (Mead
et al., 1999). It has been estimated that between 5% and 30% of
all cases of foodborne salmonellosis are caused by contami-
nated pork (Bryan, 1980, 1988; Baird-Parker, 1994).
Although intervention strategies to assure food safety can
be applied at all levels of the pork production chain, emphasis
has been placed on the potential for reduction of meat con-
tamination by minimizing contaminants at the preharvest
infected at the farm and carrying the pathogen into the abat-
toir can decrease contamination of final products. However,
an in-depth understanding of the on-farm ecology and epi-
demiology of Salmonella is fundamental to identify strategic
intervention points. A critical step in this endeavor consists in
ubclinical Salmonella infections in pigs constitute
an important food safety problem, as carrier animals pose
identifying risk factors as a precursor to the development of
monitoring and intervention (control) strategies.
Many on-farm studies have been conducted, and consid-
erable data published on Salmonella prevalence in pigs. A
number of cross-sectional studies have broadly investigated
on-farm risk factors for Salmonella infections in pigs, and a
variety of potentially contributing factors have been found,
previous cases of clinical salmonellosis, bowl-type drinkers,
dry feeding, pelleted feed, Salmonella-positive breeding herd,
solid or partially slatted floors, reduced floor space allowance,
persistent floor contamination, coinfections (with Lawsonia in-
tracellularis or porcine reproductive and respiratory syndrome
virus), lack of hygiene and biosecurity practices, contact be-
tween pigs in adjacent pens, continuous flow system, multiple
pig suppliers, environmental temperature fluctuation, and
Salmonella-contaminatedfeed(Berends etal., 1996; Davies etal.,
1997; van der Wolf et al., 1999, 2001; Funk et al., 2001; Kranker
et al., 2004; Nollet et al., 2004; Bahnson et al., 2006; Farzan et al.,
1Livestock Behavior Research Unit, Agricultural Research Service, U.S. Department of Agriculture, West Lafayette, Indiana.
2Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames,
FOODBORNE PATHOGENS AND DISEASE
Volume 6, Number 7, 2009
ª Mary Ann Liebert, Inc.
Salmonella infection reported clearly illustrates the complexity
of the on-farm ecology of this foodborne pathogen. This sce-
methods to precisely define determinants (or effectors) in the
dynamic Salmonella epidemiology within swine production
systems. Therefore, to be able to design adequate intervention
strategies, potential risk factors for the occurrence of infections
need to be individually investigated. In this study, we focused
on a single potential risk factor and evaluated it by applying
two prevalence estimate approaches (i.e., bacteriology and se-
Owing to the variability of individual growth patterns
production operations to remove animals for market over a
period of time (USDA, APHIS, 1996). Conventionally, the
heaviest pigs would be removed first (‘‘first pull’’), thus al-
lowing more time for the lighter pigs to reach a targeted
market weight (‘‘close out’’). This practice is known as split
marketing (i.e., splitting groups to be delivered toharvest into
multiple shipments over time). Research has shown that by
removing up to 50% of the heaviest pigs from a pen, growth
performance of the remaining animals is increased (Bates and
Newcomb, 1997; Woodworth et al., 2000; DeDecker et al.,
2005). Removingpigs from a pen results in anincrease in floor
and feeder space for the remaining animals, but also changes
the social dynamic of the group (Meese and Ewbank, 1973;
Fernandez et al., 1994; Tuchscherer et al., 1998). There is some
concern that this marketing strategy may serve as a potential
stressor to the remaining animals causing the reactivation of
latent infections and=or increased predisposition to new in-
Therefore, this study was designed to compare the Salmo-
nella enterica prevalence in the first group of pigs selected for
harvest (first pull) versus the last group of pigs selected for
pigs pose a higher risk of Salmonella contaminations. A sec-
bacteriologic and serologic Salmonella prevalence estimates,
which are commonly applied in monitoring programs.
Materials and Methods
Two finishing farms containing multiple production sites,
included in this study. Each production farm was visited
multiple times (four paired samplings from farm A and five
paired samplings from farm B). Each paired sampling con-
first pull (i.e., the first group of pigs selected to harvest) and
the close out (i.e., the last group of pigs selected to harvest). In
each sampling, 45 individual fecal samples were collected
directlyfromtherectum (twotothree pigsrandomlysampled
per pen). At the abattoir, the same groups of pigs were fol-
lowed, and individual meat samples (diaphragm, 40–70g)
interval between first pull and close out groups was the same
for all lots in both farms (4 weeks).
Each fecal sample (10g) was inoculated into 90mL of tetra-
thionate broth, and incubated at 378C for 20–24 hours. From
the primary enrichment, 0.1mL was transferred into 10mL of
Rappaport-Vassiliadis broth containing 20mg=mL of novobi-
ocin (Sigma Chemical, St. Louis, MO), and incubated at 428C
for 20–24 hours. After incubation, an aliquot (1mL) of the last
enrichment was analyzed for the presence of Salmonella using
a antigen-capture ELISA (Assurance?Gold EIA Salmonella,
BioControl Systems, Bellevue, WA), previously evaluated in
our laboratory (98.9% sensitivity and 96% agreement with
culture method) (Rostagno et al., 2001). All bacteriologic
mediaused duringthesampleprocessing wereobtained from
Becton Dickinson Microbiology Systems (Sparks, MD).
Individual meat samples were kept frozen (?208C) until
processed. Samples were then thawed, and the resulting fluid
(meat juice) was collected for each sample (1mL) and ana-
lyzed for the presence of anti-Salmonella antibodies using
an indirect ELISA (HerdChek?Swine Salmonella; IDEXX
Laboratories, Westbrook, ME), based on lipopolysaccharide
antigens (Camitz et al., 2001). The cut-off value (S=P ratio)
applied was 0.25, according to manufacturer’s recommenda-
Samplesize wasdetermined, basedonapopulationof1000
pigs per lot=barn with an expected prevalence of 10–15%,
with a precision of 10%. The number of replicates per farm
was determined by power analysis (minimum of four repli-
cates per farm required). Salmonella bacteriologic and sero-
logic prevalence and respective 95% confidence interval (CI)
were determined for each group sampled, and overall. Pro-
portions were compared by chi-square test, and the statistical
significance level applied for inferences was p<0.05. Ad-
ditionally, prevalence data for each matched groups of pigs
harvested (first pull and close out; n¼9) were subjected to a
hypothesis test to determine if the prevalence in the different
groups of pigs (i.e., difference between dependent groups)
was statistically equal (p>0.05) or different (p<0.05), by
applying the nonparametric Wilcoxon’s t-test. Correlation
between group-matched fecal prevalence (i.e., bacteriology)
and seroprevalence was determined using the nonparametric
statistic for correlation Spearman’s rho (JMP 4.0.0; SAS In-
stitute, Cary, NC).
All finishing barns=lots studied were Salmonella positive,
based on sampling from first pull and close out, both through
bacteriologic and serologic analysis. There was no difference
between production farms sampled for the bacteriologic and
prevalence, based on fecal samples, was 43=405 (10.6%; 95%
CI 6.03–15.2%) for first pull groups, and 80=405 (19.8%; 95%
CI 11.3–28.2%) for close out groups. Based on meat juice
samples (i.e., serology), the Salmonella prevalence for first
pull groups was 85=450 (18.9%; 95% CI 12.7–25.1%), and
226=450 (50.2%; 95% CI 26.8–73.6%) for close out groups. The
differences between first pull and close out groups in overall
statistically significant (p<0.05) in both cases (using chi-
square test to compare proportions). Median prevalence for
first pull and close out groups was 11.1% and 17.8% (bacte-
riologic), and 20% and 48% (serologic), respectively.
When considering the individual groups studied, a bacte-
riologic prevalence increase from first pull to close out oc-
curred in 7=9 (77.8%), whereas in only one group (11.1%) the
prevalence decreased, and in one group (11.1%) the preva-
lence was the same for both groups (Fig. 1). Similarly, a
serologic prevalence increase from first pull to close out
866ROSTAGNO ET AL.
occurred in 7=9 (77.8%), whereas in two groups (22.2%) the
prevalence decreased (Fig. 2). The minimum and maximum
bacteriologic prevalence in first pull and close out groups was
2.2% and 20%, and 11% and 35.6%, respectively. The mini-
mum and maximum serologic prevalence in first pull and
close out groups was 8.1% and 30%, and 30.5% and 96%,
When considering each sampled lot as the experimental
unit (n¼9), the statistical comparison of the two treatments
(i.e., first pull vs. close out) using the t-test also revealed sta-
tistically significant (p<0.05) differences between treatments
for both bacteriologic and serologic prevalence.
Overall, combining first pull and close out groups resulted
in a bacteriologic prevalence of 123=810 (15.2%), and a sero-
logic prevalence of 311=900 (34.6%), which differed statisti-
cally (chi-square test; p<0.05). Of the total 18 paired fecal and
meat samplings conducted, 14 (77.8%) had higher serologic
prevalence, whereas 3 (16.7%) had higher bacteriologic
prevalence, and only 1 (5.6%) had equal bacteriologic and
serologic prevalence estimates (Fig. 3). The correlation
(Spearman’s rho) between fecal bacteriologic culture and
meat juice serology prevalence estimates was moderate (0.48;
In the present study, split marketing was associated with a
significant increase of Salmonella prevalence from first pull to
close out groups of finishing pigs harvested. There are two
potential explanations for the increase in Salmonella preva-
lence between first pulls and close outs: (1) the reactivation of
latent infections and subsequent increased transmission, due
to the stress caused by the social disruption consequent to the
removal of the heaviest pigs from the pens (and most likely,
the dominant pigs from each group) and (2) mechanical
transmission (i.e., dissemination or spread) of the bacteria by
the personnel entering the barns to select and remove the
heaviest pigs from the pens. Although no definitive evidence
exists, it may also be possible that increased concentration of
the infected animals in the population may have occurred, if
the growth performance of subclinically Salmonella-infected
pigs was detrimentally affected by the infection (which re-
mains to be clinically demonstrated). However, based on
the serologic prevalence increase observed between groups
within the studied farms, it is more likely that new infections
occurred due to the transmission of the bacteria between the
pigs and=or through the personnel involved in the selection
and removal of the heaviest pigs.
According to the USDA=APHIS (1996), delivery of uniform-
sized pigs for harvest is very important for pork producers,
with most operations (96%) frequently assembling uniform
groups for market based on weight. These data underscore the
importance of the results reported here and its potential food
safety implications. To our knowledge, this is the only study
addressing split marketing as a risk factor for Salmonella in-
fection in finishing pigs. Although a number of studies have
been conducted to determine risk factors for Salmonella infec-
tion in commercial swine herds (Berends et al., 1996; Davies
et al., 1997; van der Wolf et al., 1999, 2001; Funk et al., 2001;
Kranker et al., 2001; Leontides et al., 2003; Beloeil et al., 2004; Lo
Fo Wong et al., 2004; Nollet et al., 2004; Bahnson et al., 2006;
Farzan et al., 2006; Mejia et al., 2006), none has included the
variable (or risk factor) investigated in this study. Further, our
results serve to illustrate how dynamic the ecology and epi-
demiology of Salmonella can be in swine populations, and how
it can be affected by simple management practices at the farm.
It is critically important to know how results from bacte-
riologic and serologic diagnostic methods correlate under
field conditions, and particularly, how well serologic results
reflect the current infection status in herds and groups of pigs
nine matched groups of first pull and close out finishing pigs,
based on fecal samples. White bars, first pull; black bars,
Bacteriologic prevalence of Salmonella enterica in
groups of first pull and close out finishing pigs, based on
meat juice samples. White bars, first pull; black bars, close
Serologic prevalence of S. enterica in nine matched
0 102030 405060 708090 100
lence of S. enterica for 18 groups of finishing pigs.
Scatter plot of bacteriologic and serologic preva-
SPLIT MARKETING EFFECT ON SALMONELLA IN SWINE867
delivered to abattoirs. The overall prevalence estimates ob-
tained in this study by applying the two diagnostic tools (i.e.,
bacteriology and serology) differed markedly, with an overall
higher serological prevalence estimate (15.2% vs. 34.6%, re-
spectively). Our results are in agreement with previous on-
farm studies reporting discrepancies between bacteriologic
and serologic prevalence estimates, with serologic estimates
being higher than bacteriologic estimates (Stege et al., 2000;Lo
Fo Wong et al., 2003; Hurd et al., 2004; Funk et al., 2005).
However, when comparing bacteriologic and serologic
prevalence estimates, it has to be kept in mind that a temporal
disassociation exists between infection and serologic re-
sponse. Recent Salmonella infections (i.e., less than 5–7 days)
usually cannot be detected by serologic analysis. Therefore, it
is possible that pigs infected during the last days of the fin-
ishing production stage are not serologically detected, when
samples are collected at slaughter. More importantly, it is
possible that animals with positive serological status (which
has been shown to persist for several weeks; Nielsen et al.,
1995) do not continue to shed Salmonella in the feces and,
therefore, would not be detected with bacteriologic analysis.
This scenario would explain the common finding of higher
serologic prevalence estimates, as reported here, and by others
(Stege et al., 2000; Lo Fo Wong et al., 2003; Hurd et al., 2004;
Funk et al., 2005). Studies with experimentally infected pigs
have shown that the onset of serologic response and peak
seroprevalence occur at approximately 7 and 30 days post-
and probably, do occur, under natural conditions. This ob-
servation may occur because pigs within groups are infected
at different points in time with variability in both exposure
rate and level, and in individual host responses. Moreover,
group of pigs (i.e., lot or barn) will further complicate this
response are serovar dependent (van Winsen et al., 2001).
The effective identification and evaluation of risk factors
and intervention measures, and the development and im-
plementation of reliable preharvest monitoring and control
programs depend on the ability to accurately assess the Sal-
monella status of animal groups or populations. However, the
diagnostic tools currently available for preharvest investiga-
tions of Salmonella are limited. Despite the known limitations
of fecal bacteriologic culture for determination of Salmonella
status (Funk et al., 2000; Hurd et al., 2004), it remains the gold
standard for on-farm Salmonella investigations. Estimates of
its sensitivity are frequently low to moderate. In the other
hand, serologic methods have the ability to assay a large
number of samples rapidly and at relatively low cost, as is
necessary in monitoring and control programs. However,
considering that the presence of antibodies reflects previous
exposure to Salmonella rather than current infection, the rela-
tionship between serologic status and microbial risk at har-
vest is less evident than with preharvest bacteriologic culture.
Asymptomatic carriage (i.e., subclinical infection) and in-
most Salmonella-infected pig herds. Identification of risk fac-
tors that may influence the prevalence of this intestinal car-
riage is critical for development of effective intervention
measures to reduce Salmonella contamination of market pigs.
As our knowledge on the ecology and epidemiology of Sal-
monella in swine populations evolves, the effect of multifac-
torial issues becomes evident underlying the complexity of
the microbial preharvest food safety risks challenging the
pork industry. The perimarketing stage of the pork produc-
tion chain (i.e., when pigs are removed from the production
farms and transported to the abattoirs for slaughter and
processing) includes a multitude of variable factors that make
interactions. Research to investigate the effect of each com-
ponent of the perimarketing complex stage is needed, par-
ticularly under more controlled conditions. This study
demonstrates for the first time (under commercial conditions)
that a significant increase in Salmonella prevalence occurs be-
tween the first and the last group of pigs harvested from
finishing lots, when a split marketing strategy is practiced.
Therefore, we conclude that close out groups of market pigs
constitute a higher risk for Salmonella contamination of the
abattoir environment, and potentially, of pork products.
The authors thank Robert Schneider, Carol Wiltsey, and
Adrienne Norgrant for technical assistance, and the partici-
pating pork producer for collaborating in this research.
Mention of trade names or commercial products in this
article is solely for the purpose of providing specific infor-
mation and does not imply recommendation or endorsement
of the U.S. Department of Agriculture.
No competing financial interests exist.
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Address correspondence to:
Marcos H. Rostagno, D.V.M., MPVM, Ph.D.
Livestock Behavior Research Unit
Agricultural Research Service
U.S. Department of Agriculture
125 S. Russell St.
West Lafayette, IN 47907
SPLIT MARKETING EFFECT ON SALMONELLA IN SWINE869