Preharvest Food Safety in

Broiler Chicken Production

WALID Q. ALALI1 and CHARLES L. HOFACRE2
1
College of Public Health, Hamad bin Khalifa University, Doha-Qatar; 2Department of Population Health,
Poultry Diagnostic and Research Center, University of Georgia, Athens, GA 30602

ABSTRACT Preharvest food safety in broiler production is a Campylobacter infections, respectively, occur annually
systematic approach to control the introduction, propagation, (3). Both pathogens are frequently associated with the
and dissemination of Salmonella and Campylobacter from
consumption of contaminated poultry products. It is
breeder flocks to the end of their progeny (broilers) life cycle.
New and revised more stringent performance standards for
estimated that 10 to 29% of Salmonella infections and
these pathogens at the processing plant level require 43% of Campylobacter infections are associated with
continuous evaluation of the preharvest management practices poultry products (4–7).
and intervention strategies used by the poultry industry. Poultry meat production and consumption is of sig-
The implementation of stricter biosecurity plans, vaccination nificant economic importance in many countries world-
of breeder flocks for Salmonella, and usage of feed that is free wide. Poultry is the second most consumed meat (33%
of animal by-products are some of the measures recommended of all meats) globally, after pork (37%) (8). However,
to control the pathogens. Interventions shown to be effective
poultry is the fastest growing meat sector as reflected by
in experimental settings need to be assessed for their
cost-effectiveness and efficiency when applied at the farm level. the increase in world consumption. The consumption
of poultry meat increased by 14.4% from 2004 to

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2008 (from 80 million tons in 2004 to 93 million tons
INTRODUCTION in 2008). While the consumption increased slightly in
The goal of preharvest broiler food safety is to mini- the United States (2.9%), it increased by 25% in China.
mize opportunities for the introduction, persistence, and The United States is ranked number one in poultry meat
transmission of foodborne pathogens (mostly Salmo- production, followed by China and Brazil. However,
nella and Campylobacter) in the bird flock. Current in- the largest exporters of poultry meat are Brazil and the
tervention strategies to combat foodborne pathogens United States.
in preharvest broiler production target Salmonella and With such increasing poultry meat production and
Campylobacter in general, or more specifically target consumption worldwide, the safety of poultry products
certain serotypes that are most frequently associated is a priority to consumers, producers, and government
with human disease. regulators. Poultry meat has been identified as one of the

Received: 2 June 2014, Accepted: 31 March 2016,

Published: 19 August 2016
OVERVIEW OF SALMONELLA AND Editors: Kalmia Kniel, Department of Animal and Food Science,
CAMPYLOBACTER INFECTIONS IN HUMANS University of Delaware, Newark, DE; Siddhartha Thakur, North
THAT ARE LINKED TO POULTRY PRODUCTS Carolina State University, College of Veterinary Medicine, Raleigh,
NC
Salmonella and Campylobacter infections are a signifi- Citation: Alali WQ, Hofacre CL. 2016. Preharvest food safety in
cant public health concern in the United States and broiler chicken production. Microbiol Spectrum 4(4):PFS-0002-
worldwide (1–3). In the United States, the Centers for 2014. doi:10.1128/microbiolspec.PFS-0002-2014.
Correspondence: Walid Q. Alali, [email protected]
Disease Control and Prevention (CDC) estimated that
© 2016 American Society for Microbiology. All rights reserved.
1.03 million and 0.8 million cases of Salmonella and

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Alali and Hofacre

most significant food vehicles for Salmonella and Cam- identified Campylobacter serovars associated with hu-
pylobacter. For instance, in the United States, an esti- man infections in the United States were Campylobacter
mated 100,000 to 300,000 cases of human salmonellosis jejuni and Campylobacter coli (17–19). C. jejuni is the
each year have been attributed to the consumption of most common serovar associated with poultry products,
contaminated poultry products. Despite the control and followed by C. coli (20–23).
intervention strategies established to control Salmonella
contamination in processed poultry, the U.S. Depart-
ment of Agriculture (USDA) Food Safety and Inspection STRUCTURE OF INTEGRATED POULTRY
Service (FSIS) reported a 4.3% Salmonella prevalence PRODUCTION SYSTEM IN
on raw broiler carcasses in poultry processing plants in THE UNITED STATES
2012 (9). Since the United States produces an estimated It is necessary to understand the integrated broiler pro-
8.9 billion broiler birds a year, around 382 million duction system to better understand the transmission
carcasses can be contaminated each year. The latest dynamics of Salmonella and Campylobacter as well as
estimate in 2011 from a USDA-FSIS microbiological the development and application of management strat-
baseline data collection survey revealed that Campylo- egies and intervention methods. The poultry industry in
bacter contamination prevalence on broilers was 9.4% the United States and in many countries worldwide is a
(10). vertically integrated production, processing, and distri-
The per capita consumption of poultry products bution system. Most poultry companies in the United
has increased 6.5-fold since 1910 (11). An increase in States have contract agreements with farmers (growers)
consumption of poultry increases the potential risk for that bind farmers to grow birds (breeder or broilers)
exposure to Salmonella and Campylobacter through in exchange for payment. Operating expenses such
contaminated poultry products unless steps are taken as repairs and maintenance, clean-up cost, manure,
to improve the microbiological safety of the products. and dead bird disposal are the responsibility of the
The most commonly identified Salmonella serovars farmer. Most integrators require houses to be built
associated with human infections in the United States and equipped according to strict specifications. The
were Salmonella enterica Enteritidis, Typhimurium, poultry companies control the rest of the production
Newport, Javiana, I 4,[5],12:i:-, Montevideo, Heidelberg, processes, which include providing chicks to the farmers
Muenchen, Infantis, and Braenderup (12). According to a growing breeders (parent stock) or broiler flocks; pro-
USDA-FSIS report in 2011, the top serovars associated ducing and distributing feed; providing veterinary and
with broiler carcasses were S. enterica Kentucky, Ente- management services to the farms; hatching the breeder-
ritidis, Typhimurium, Infantis, Heidelberg, Johannesburg, broiler eggs; transporting broiler birds to the processing

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4,[5],12:I:-, 8,20:-:z6, Mbandaka, and Berta (13). Al- plant; and processing, production, and marketing of
though it’s not commonly associated with human infec- broiler meat.
tion, S. Kentucky has been identified as the most common
serotype isolated from broilers (51.8% of Salmonella de-
tected on carcasses) and retail chicken breasts (25.3%) USDA-FSIS NEW STANDARDS FOR
(13, 14). S. Kentucky was recently identified as a potential SALMONELLA AND CAMPYLOBACTER
emerging multidrug-resistant human pathogen in Europe The USDA-FSIS implemented new performance stan-
and North Africa because the numbers of cases have risen dards for Salmonella, and for the first time, standards
significantly over the last decade (15). In the United States, for Campylobacter on broiler carcasses at slaughter/
S. Kentucky increased from averaging about 62 cases per processing plants became effective 1 July 2011. The
year in 1996 to 2004 before climbing to 123 cases in 2006 number of samples collected (n = 51) for broiler patho-
(12). The prevalence of multidrug-resistant S. Kentucky gen verification remains the same as before; however,
in poultry is also alarming; according to National Anti- each carcass is now analyzed not only for Salmonella,
microbial Resistance Monitoring System data for 2007, but also for Campylobacter. A processing plant passes
50% of isolates from broiler meat that were resistant to the Salmonella and Campylobacter standards if no
≥5 antimicrobials were identified as S. Kentucky (14). more than 5 and 8 positive samples, respectively, in a
Unlike Salmonella, the State Public Health laborato- 51-sample set for broilers are detected. If a plant fails
ries that participate in the CDC FoodNet surveillance to meet these standards, the FSIS issues a warning and
program do not serotype Campylobacter isolates (16). collects a follow-up 51 samples and analyzes them for
Based on the scientific literature, the most commonly both pathogens.

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 Preharvest Food Safety in Broiler Chicken Production

The New Salmonella Standards for Broilers susceptibility of the birds, stress due to overcrowding
Based on the latest microbiological baseline survey of or underlying illness, level of pathogen exposure and
broiler carcasses (2011–2012), FSIS estimates of Sal- virulence of the organism to facilitate colonization
monella prevalence on post-chilled carcasses was 4.3% and/or evade host defenses, and competition with gut
(9). With a goal of further reduction of human illness microbiota for colonization sites (19, 24, 25). Broilers
associated with chicken products, the FSIS issued these are most susceptible to pathogen colonization during
new standards to improve pathogen control in process- the first few days of hatch by vertical transmission from
ing plants. The FSIS believes that the standard of no infected parents or by horizontal transmission at the
more than 5 positives out of 51 samples will lead to an hatcheries during feeding, handling, and transportation
80% probability that a processing plant will meet a (24, 26, 27). Additionally, birds are highly susceptible to
7.5% performance standard. The qualitative (presence/ Salmonella and Campylobacter infections during feed
absence) Salmonella testing method will continue as be- withdrawal prior to slaughter due to stress, consump-
fore, using the 400-ml carcass rinse to determine which tion of contaminated litter, and alterations of the crop
carcasses are positive. The FSIS predicts that in the first pH and intestinal microbiota (28–30). Preharvest inter-
two years of implementing the new standards for Salmo- ventions to control Salmonella and Campylobacter in
nella for broilers, a reduction of approximately 26,000 broilers should be directed largely at the most critical
human cases will occur compared to the old standards points for pathogen introduction to the flock. In this
(i.e., no more than 13 positives out of a 51-sample set). section, we discuss the different routes of Salmonella and
Campylobacter entry to broiler flocks and possible in-
The New Campylobacter Standards for Broilers tervention methods.
In the microbiological survey in 2011, the FSIS collected
quantitative and qualitative data for Campylobacter Feed Contamination and Recontamination
on broiler carcasses. The FSIS estimate of Campylo- Feed in general is considered a vehicle for foodborne
bacter prevalence on postchilled carcasses was 9.4%. pathogen transmission in food animal production, and
The agency uses a direct plating method (1 ml of car- in poultry production in particular. Poultry birds that
cass rinsate) to quantify (enumerate) Campylobacter, consume contaminated feed could get infected and col-
as well as a qualitative (enrichment) method using 30 ml onized with pathogens, resulting in pathogen coloni-
of rinsate to detect the organism when direct plating is zation and fecal shedding in the farm environment.
negative. The 1-ml direct plating test procedure is less Although the poultry industry understands the role and
sensitive than the 30-ml procedure, but it detects a high importance of feed as a vehicle of foodborne pathogen
level of contamination. The performance standards for transmission in poultry production, contamination of

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Campylobacter will be based on the results from the feed at the mill continues to be a problem since con-
two detection methods: the number of samples that are trol and/or elimination of contaminants is considered
positives based on the 1-ml method and the combined a daunting task. There are several challenges involved
percentage of positive results of either the 1-ml and/or with detection of Salmonella and/or Campylobacter
the 30-ml methods. in poultry feed: (i) organisms are not uniformly dis-
The performance standard for the 1-ml method is no tributed in feed; (ii) organisms might be damaged or
more than 8 positive samples of the 51-sample set, injured, making them difficult to isolate/detect; (iii) mi-
whereas the performance standard for results of both crobiological and molecular laboratory methods have
methods is no more than 27 positive of 51 samples. The detection limits, especially for dry sample matrix; and
FSIS predicts that in the first two years of implementing (iv) deciding on the number of samples to collect for
the new standards for Campylobacter for broilers, a re- microbial analysis as well as the sample analytical vol-
duction of approximately 39,000 human cases will oc- ume is a challenge. That being said, the goal of pathogen
cur compared to prior implementation of the standards. control in feed should be to ensure that feed contam-
inants are below a certain level (i.e., threshold) which
will pose minimal risk to human and bird health. This
CONTROL OF FOODBORNE PATHOGENS can be achieved by following “sound and practical”
IN BROILER PRODUCTION SYSTEMS microbial sampling plans, good manufacturing prac-
AT THE PREHARVEST LEVEL tices, and application of intervention strategies such as
Several factors can affect Salmonella and Campylobac- chemical and physical treatments to control pathogens
ter colonization in broilers, including the age and genetic in feed.

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Alali and Hofacre

It has been reported that poultry feed is often con- the microbiological quality of feed should be considered
taminated with a variety of pathogens such as Salmo- when needed.
nella spp. and Enterococcus (31, 32). Feed is mostly free Several chemical and physical interventions have been
of Campylobacter since feed is dried and pelleted under applied to feed to prevent and control Salmonella con-
high temperature; therefore, the survival of this organ- tamination. These methods include treating feed with
ism in feed is unlikely (33, 34). Animal feed manufac- acids (e.g., organic and propionic acids) and formalde-
turing and distribution is a multistage process as follows: hyde, heat treatments, and irradiation (36–39). Combi-
(i) in the field (preharvest) with plant crop (e.g., corn and nations of acids and heat treatments are common in
soybean) processing as well as production of protein the poultry feed industry because they have been proven
meals (e.g., animal, bone, and fish); (ii) at the feed mill to effectively reduce the level of Salmonella in the end
(i.e., harvest), where feed goes through grinding, mixing, product (40).
pelleting, and then storage at the mill; and (iii) in post-
harvest, which includes transportation of feed to animal Breeder Flocks (Parent Stock)
farms, storage at the farms, and dispensing of feed to Vaccination programs for breeder flocks are becoming
animals for consumption. Bacterial contamination of part of the regular food safety control system in most
animal feed can occur at various manufacturing stages. poultry companies in the United States and the European
Control of pathogens in raw feed ingredients and during Union. The goal of vaccination in broiler breeder farms
production has the most significant impact on feed con- is to reduce the vertical transmission of Salmonella spp.
tamination. At the feed mill, poultry feed can become to the hatching progeny and ultimately to reduce the
contaminated during manufacture/processing as a result incidence of the organisms being carried into the pro-
of cross-contamination. The most critical point for mi- cessing plant. Jones et al. (41) surveyed Salmonella con-
crobial contamination and growth at the feed mill is tamination in broiler production and processing systems
the pellet cooler. The combination of moisture and heat in the United States. They observed similar rates of con-
is a favorable environment for microbial survival and tamination in fecal droppings collected from breeder
growth. The heating process during production is re- houses, day-old chicks, and live birds in broiler houses.
quired to pellet the feed, which usually kills most path- They suggested that the breeder house environment is an
ogens in the produced feed. Inadequate temperature for important vehicle for the transmission of contamination
the pelleting equipment and feed conditioner would in- to the final product.
crease the likelihood of microbial survival. For Salmonella, the two types of vaccinations used for
Contamination of feed before and after the heating breeder flocks are inactivated (killed) and live-attenuated.
point is common and can be attributed to many factors Both types of vaccines have demonstrated effectiveness

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within the feed mill facilities. These include unclean re- in controlling Salmonella spp. transmission to broiler
ceiving and unloading area, unclean intake pits, dust chicks (42–45). Live-attenuated vaccines are used to pro-
generated by the feed ingredients, dirty conveyers with vide hens with long-term immunity against Salmonella
leftover feed from previous loads, inadequate feed stor- spp. colonization, whereas killed vaccines provide im-
age conditions, and presence of visitors in unsanitary munity that passes from the hen into the eggs. Some
cloths (35). Feed ingredients should be inspected prior poultry companies use both types of vaccine for better
to unloading for signs of rodent contamination, bird immunity against Salmonella in breeder broiler birds.
droppings, and insect infestation. Inspection is par- A recent study compared poultry companies that
ticularly important given the difficulty of testing large vaccinated their breeders with live-attenuated S. Typhi-
amounts of incoming ingredients and of testing the feed murium followed by a booster dose of killed Salmonella
during and after production. This due to the cost, time, vaccine (S. Berta and S. Kentucky) to companies that
and labor associated with the microbial analysis. There- did not vaccinate (45). The authors reported that vac-
fore, feed mills should consider investigating which sup- cinated breeder birds had significantly lower prevalence
pliers have been consistent and reliable in delivering of Salmonella in the ceca (38.3% versus 64.2%) and
ingredients without macro and/or micro levels of con- the reproductive tracts (14.22% versus 51.7%) when
tamination. The poultry industry may avoid using high- compared to nonvaccinated breeders. Furthermore, the
risk Salmonella-contaminated ingredients such as animal authors found that broiler progeny chicks from vacci-
by-products to reduce the likelihood of contaminated nated breeders had significantly lower Salmonella prev-
feed. Microbial sampling plans designed to determine alence (18.1%) compared to chicks from nonvaccinated
the minimum number of sampling units that represent breeders (33.5%). Moreover, breeder vaccination was a

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 Preharvest Food Safety in Broiler Chicken Production

significant factor associated with lower environmental dust) which may contain Salmonella. This pathogen can
Salmonella contamination of broiler chicken farms. The contaminate the outer surface of the egg shell and may
authors also followed the birds to processing plants, penetrate the shell and multiply inside the egg (60).
where they found a significantly lower Salmonella prev- Commercial hatcheries are considered a major source
alence on broilers (from vaccinated breeders) entering of Salmonella infection of young chicks (61–63). This is
the processing plants (23.4%) compared to nonvac- mainly because Salmonella-negative chicks are exposed
cinated flocks (33.5%). In another study, Berghaus et al. to Salmonella-positive chicks in a confined environment.
(44) compared breeder flocks that were vaccinated with The dust generated from contaminated eggs and the fluff
a killed Salmonella vaccine (three serotypes: Typhimu- from newly hatched chicks can widely spread Salmo-
rium, Enteritidis, and Kentucky) to breeder flocks that nella in the hatchery cabinet (61–63). Researchers re-
were not vaccinated. They reported that vaccinated ported that Salmonella was detected on 71% of eggshell
breeder flocks had significantly higher humoral im- fragments, on 80% of swabs from the chick conveyor
munity, and their progeny had significantly lower Sal- belt, and on 74% of chick tray liners that contained
monella prevalence and numbers compared to their feces (61). In another study, Byrd et al. (64) reported a
nonvaccinated counterparts. However, vaccination of 12% Salmonella prevalence (n = 700 chick tray liners
breeders did not significantly reduce the environmental tested) in hatcheries. Epidemiological studies have dem-
Salmonella contamination of breeder farms. Poultry onstrated a link between Salmonella isolates from the
companies are encouraged to vaccinate their breeder hatchery and the isolates found on processed chicken
flocks with live-attenuated and/or killed vaccine, espe- carcasses. Bhatia and McNabb (65) followed Salmonella
cially if the company has a history of high prevalence contamination from the hatchery to the processing plant
of Salmonella in their broiler flocks and/or at the pro- and found that the same Salmonella serotype was
cessing plant. detected in fluff and meconium samples collected at the
Regarding Campylobacter vaccine programs for hatchery, in litter samples at the broiler farm, and on
breeders, researchers revealed that development of live- carcasses following processing.
attenuated vaccine has been hampered by the genomic Interestingly, hatcheries are considered a minor source
and phenotypic instability of this organism (46, 47). of Campylobacter transmission and infection of chicks
Researchers have used S. Typhimurium engineered genes (66). This organism was detected in 0.75% (n = 2,000)
that delivered immunity to Campylobacter, but with lim- of tray liners of day-of-hatch broiler chicks collected
ited success (48–50). Furthermore, other types of Cam- from eight commercial hatcheries (66). Vertical trans-
pylobacter vaccines have been investigated. It has been mission of Campylobacter from breeder hens to their
demonstrated that killed and flagellin-based Campylo- progeny is not well understood. A number of experi-

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bacter vaccines do not possess an effective immune re- mental studies revealed that breeder hens can potentially
sponse to protect chickens from colonization with this transmit Campylobacter vertically through eggs (67–71).
organism (51–55). Campylobacter resides in the muco- Furthermore, Cox et al. (72) found that Campylobacter
sal layer of the chicken intestine, so it might not stimu- isolates from breeder hens’ fecal samples had identical
late enough immune response to provide protection ribotype patterns to those isolates from their offspring’s
(46). To date, no Campylobacter vaccine that is effective fecal droppings. These authors suggested that hatching
in commercial poultry settings has been developed for cabinets and the hatchery environment can be a source
breeder or broiler flocks. of Campylobacter contamination and transmission to
newly hatched birds.
Hatchery Hatcheries employ a number of interventions to con-
Broiler eggs can be contaminated at the breeder farm trol the transmission of these pathogens. These include
and at the hatchery (56). The hatching chick might be disinfection of the incubator and hatching cabinet sur-
infected with Salmonella spp. through vertical and/or faces as well as disinfection of the hatching eggs using
horizontal transmission. Vertical transmission occurs UV light, ozone, electrostatic charging, and electrostatic
when breeder hens with contaminated reproductive spraying (73–77).
tracts lay fertile broiler eggs that harbor Salmonella (57,
58). Horizontal transmission can occur when contami- Farm and Farm Environment
nated eggs are hatched and Salmonella spreads among There is a wide array of potential routes of Salmo-
newly hatched chicks (59). At the farm, laid eggs are nella and Campylobacter infection of broilers as well
exposed to environmental contaminants (e.g., feces and as intervention methods to control these pathogens at

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Alali and Hofacre

broiler farms. In this section we will discuss (i) the role nella prevalence in litter treated with sulfuric acid (85).
of poultry litter in pathogen transmission and control Furthermore, Williams (84) found that the use of 4 or
methods, (ii) the association between the feed with- 6% formalin to spray litter led to elimination of Sal-
drawal period and pathogen colonization as well as monella from the litter surface. The effect of citric,
control methods, (iii) biosecurity measures at the farm tartaric, and salicylic acids on pathogens in poultry
to control infection of broiler flocks, (iv) antimicrobial litter was assessed in an experimental trial (81). The
use and pathogen prevalence in flocks, and (v) prebiotic authors reported a significant reduction in S. Enteritidis
and probiotic use to control these pathogens in flocks. prevalence, with salicylic acid being the most effective.
However, other studies reported less effect of litter
Litter amendments on pathogen prevalence. Line’s (82) ex-
Litter is the absorbent bedding material used to cover perimental study revealed that two products (sodium
the floor of a broiler chicken house. Depending on the bisulfate and aluminum sulfate) did not significantly
availability of materials, litter can be made of wood reduce Salmonella prevalence in poultry litter, but they
shavings, pine straw, peanut hulls, and other dry, ab- did for Campylobacter. Similarly, Pope and Cherry (83)
sorbent, low-cost materials. Used litter consists of a large did not find a significant Salmonella reduction when
amount of feces, feathers, and spilled feed and high levels they applied sodium bisulfate to litter.
of moisture. In the United States, the litter is generally Interestingly although one would expect that pro-
used for several broiler flock cycles. A fresh layer of longed use of litter with multiple broiler flocks will in-
bedding is often added to the litter prior to placement of crease pathogen contamination in the litter (85), other
a new flock. In other countries, the litter is completely studies have demonstrated the contrary. Corrier et al.
removed, and then the broiler house is cleaned and (86) found in an experimental trial that birds raised on
disinfected before placement of a new flock. Studies have used litter had higher cecal concentrations of volatile
investigated the epidemiological link between isolates fatty acid and lower prevalence of Salmonella cecal
detected on litter and contamination of broiler carcasses. colonization compared to birds raised on new litter.
Bhatia et al. (78) reported that Salmonella found on In another study, Roll et al. (87) followed Salmonella
broiler litter was a reliable indication of both flock in- prevalence on boot covers at broiler farms at one poul-
fection and carcass contamination. Furthermore, Bhatia try company in Brazil for 2 years. The authors reported
and McNabb (65) revealed that the same Salmonella that Salmonella prevalence on reused litter declined over
serotypes in litter samples at broiler farms were found on time.
carcasses during processing. Furthermore, Corry et al. It is recommended that farmers keep their broiler
(79) found that Salmonella serotypes detected in litter litter as dry as possible, replace the top layer of the litter

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samples during grow-out were usually detected in fewer with a new one, and apply litter amendments that are
birds at the end of the grow-out as well as in carcasses acid-based.
during processing. Goren et al. (80) surveyed broiler
production systems in The Netherlands and found a Feed withdrawal
positive correlation between the Salmonella prevalence A common practice in the poultry industry is to with-
from litter at 5-weeks of age and that from ceca at pro- draw feed before broilers are shipped to the processing
cessing. None of these studies determined the molecular plant (88, 89). Feed withdrawal (8 to 12 h preslaughter)
genetic similarity of the isolates using subtyping tech- reduces the amount of feces in the birds’ crop and gut
niques (e.g., pulsed field gel electrophoresis) from litter, and therefore reduces the potential risk of carcass con-
birds, and processing plants. tamination with Salmonella and Campylobacter during
Several types of amendments can be applied to litter processing (90–92). However, feed withdrawal has been
to reduce the emission of ammonia by modifying the shown to increase the populations of Salmonella and
litter pH. The effect of these amendments on Salmonella Campylobacter in the ceca and crops of broilers (92–
prevalence and other pathogens in the litter has been 96). As the birds search for feed during the withdrawal
the subject of a number of studies (81–85). These studies period, they consume contaminated litter, which may
examined the effect of litter amendment products such result in crop and ceca pathogen contamination. Fur-
as organic acids, formalin, sodium bisulfate, aluminum thermore, feed withdrawal has been associated with an
sulfate, and sulfuric acid on Salmonella and other path- increase in crop pH due to reduction in Lactobacillus
ogens such as Campylobacter. In an experimental study, fermentation and lactic acid. The rise in pH has been
the authors reported a significant reduction in Salmo- linked to increased Salmonella survival in the crop (94,

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 Preharvest Food Safety in Broiler Chicken Production

95). Furthermore, crops are 85 times more likely to ing the breeder and broiler houses, which include strat-
break open in a processing plant compared to ceca, egies to prevent and control wildlife, rodents, insects,
which could lead to carcass contamination with these unauthorized human visitors, and fomites (e.g., feed
pathogens (93, 94, 96). Interestingly, crops were found truck and farm equipment), because they are all potential
to be 3.5 times more likely to be contaminated with Salmonella and Campylobacter vectors/carriers.
Salmonella compared to ceca after feed withdrawal (93, Researchers have shown that darkling beetles, mites,
94). As for Campylobacter, feed withdrawal increases this and flies, commonly found in the poultry litter and
pathogen prevalence in the crop, but it did not signifi- poultry farm environment, can be vectors for Salmonella
cantly alter the Campylobacter prevalence in the ceca (92). and Campylobacter (107–114). In a broiler house, the
A number of studies have examined the effect of infestation of darkling beetles can be massive (up to
various interventions prior to or during the feed with- 1,000 insects per square meter of litter) (115). Birds can
drawal period to control pathogen contamination of the become infected with pathogens by ingesting contami-
crop and ceca. These interventions included the acidifi- nated beetles, mites, and fly larvae. Wild animals (e.g.,
cation of drinking water (97, 98), treating the drinking dogs and cats) and wild birds (e.g., waterfowl shore-
water with chlorate (99), feeding broilers a glucose- birds, and gulls) can also be vectors of foodborne path-
based cocktail (100), acidification of feed (101–104), ogens (116). Rodents (rats and mice) can be a significant
and using essential oils in drinking water (105, 106). source of Salmonella and Campylobacter in farms and
Parker et al. (98), who determined that a commercial the surrounding areas (113, 117, 118).
organic acid blend, when administered at 0.04% and Fomites such as dirt and soil were found to be con-
0.08%, significantly reduced the prevalence of Salmo- taminated with pathogens. Bailey et al. (113) found that
nella in crops and ceca (by 1.5 logs) of broiler birds soil samples collected from the entrance of broiler
compared to controls. Byrd et al. (97) also reported a houses were Salmonella-positive (6.1%, n = 131). Other
significant reduction in the percentage of Salmonella biosecurity risk factors associated with pathogen prev-
culture-positive crops from broilers treated with lactic alence at the farm were reported. In an epidemiological
acid in drinking water compared to controls. In addi- study in France, the authors revealed that the removal
tion, the authors reported that 0.5% lactic acid in water of mobile equipment inside the broiler house prior to
did not statistically lower the Salmonella prevalence in cleaning and disinfection and using specific containers
ceca compared to controls. In recent studies by Alali to collect dead birds decreased the risk of Salmonella
(105, 106), a commercial essential oil blend used in contamination in broilers (119). In another study, by
drinking water significantly reduced Salmonella coloni- Gradel et al. (120) in The Netherlands, the authors re-
zation in crops of broilers, compared to 0.44% lactic ported a link between reduced Salmonella prevalence in

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acid (97) and a 0.4% organic acid blend (98). Another broiler farms and the following factors: workers wash-
product (i.e., chlorate) was used in broiler drinking ing their hands with antiseptic soap prior to entering
water (24 to 48 h prior to slaughter) and reduced the the broiler house, proper disposal of dead birds, using
percentage of Salmonella-contaminated crops and ceca gravel around the broiler house, regularly checking on
compared to controls (99). It is important that the prod- rodent baits in the house, and the use of combined sur-
uct used in water or feed to control pathogens in crops face and pulse-fogging disinfection methods. Cleaning
and/or ceca both be cost-effective and not negatively and disinfection of broiler houses after removal of litter
impact bird health, performance (weight gain and feed was considered a significant factor that reduced Salmo-
conversation ratio), and water consumption. Treated nella contamination in the next placement flock (121).
drinking water consumption by the broilers is important However, cleaning and disinfection was not significantly
to measure. For instance, it was reported that birds con- associated with the prevalence of Campylobacter fecal
sumed less water treated with organic acid compared to shedding (122). In agreement with Gradel et al. (120),
untreated water (99). Renwick et al. (123) reported that disposal of dead
chickens by incineration or complete removal from the
Biosecurity farm premises was associated with reduced Salmonella
Biosecurity at the poultry farm can be defined as the prevalence in the farm. The practice of workers dipping
management action plans designed by the poultry com- their boots in disinfectant solution prior to entering
pany to prevent and control the introduction of patho- broiler houses, and the frequency of changing the solu-
gens into the flock. This includes action plans to prevent tion, was found to reduce colonization of birds with
and control Salmonella and Campylobacter from enter- Campylobacter (124, 125).

ASMscience.org/MicrobiolSpectrum 7
Alali and Hofacre

Poultry housing should be designed to prevent entry subtherapeutic antibiotic use in poultry farms impact the
of any vector such as rodents and wild birds. Pest-con- prevalence/level of Salmonella and Campylobacter in
trol measures such as traps and baits should be used broilers? To be able to answer this question, longitudinal
inside and outside of the house and checked regularly. epidemiological studies are needed to compare the
Human access to the house and to the farm should be prevalence and levels of Salmonella and Campylobacter
regulated. Workers’ sanitation and hygiene measures in broiler farms before and after discontinuation of
such as footbaths, hand washing, and the use of dis- antibiotics.
posable coveralls and overshoes should be implemented. Few studies have compared the Salmonella prevalence
It is recommended that sharing equipment and transport in conventional and antibiotic-free (i.e., organic/free-
vehicles with other farms should be minimal. Equipment range) broiler flocks at the farm level. Siemon et al. (131)
and vehicles should be effectively decontaminated be- and Alali et al. (132) reported significantly lower prev-
fore entering the farm environment. Stricter biosecurity alence of Salmonella at pasture and USDA-certified
measures should be employed for breeder farms/houses organic farms, respectively, compared to conventional
such as shower-in–shower-out (i.e., shower prior to and farms. Other studies of pasture broiler farms reported no
after entry to the breeder farm), or at least disposable Salmonella detection (133), low Salmonella prevalence
footwear, coveralls, and hair covering should be used. of 2.9% (135), and 25% Salmonella prevalence (155).
Salmonella- and Campylobacter-contaminated water For Campylobacter prevalence on pasture and organic
poses a low risk of pathogen transmission to poultry farms (antibiotic-free farms), the overall prevalence was
flocks. Salmonella was detected in 1.4% (n = 731) of high, ranging from 61 to 90.4% (133–136), except for
water samples collected from water lines in broiler farms Hanning et al. (137), who found that Campylobacter
(113), whereas Campylobacter was detected in 9% (n = prevalence was 30%. However, at retail, Salmonella and
100) of water line samples in broiler farms (126). Water Campylobacter prevalence on organic and antibiotic
contamination with Salmonella was associated with fe- free broilers meat has been shown to be higher and lower
cal contamination at broiler farms (123). Campylobac- than conventionally reared broiler meat (138–141).
ter is very sensitive to chlorination of water (127, 128).
However, the presence of organic materials might re- Prebiotics and probiotics
duce the effectiveness of chlorination on Campylobacter Prebiotics and probiotics are added to feed to reduce
as well as Salmonella. Studies have revealed that the pathogen colonization and subsequent shedding in poul-
addition of sanitizers (e.g., chlorine) to drinking water try. Prebiotics are nondigestible carbohydrates that stim-
might reduce the risk of a broiler flock being positive for ulate the growth and/or activity of one or more bacteria
Campylobacter (125, 129). Interestingly, Stern et al. in the gastrointestinal tract (142). Probiotics are single

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(130) found that chlorination of water at 2 to 5 ppm or multiple defined microorganisms that act as pro-
had no effect on Campylobacter colonization in broilers’ tective microflora in the gut to prevent colonization by
guts. Therefore, alternative sanitizers or possibly higher pathogens (143, 144). Competitive exclusion (CE) is a
chlorine concentrations in drinking water should be form of probiotic culture but is composed of both de-
considered; however, bird water consumption should be fined and undefined microorganisms from adult chicken
monitored and compared to untreated water. Cleaning intestines and is given via spray or water to newly
the water lines between flocks with sanitizers to destroy hatched chicks (145). Young chicks are highly suscep-
biofilms is important to improve drinking water quality. tible to infection with Salmonella and Campylobacter,
largely due their underdeveloped intestinal microbial
Antibiotic use populations. Therefore, administration of CE enhances
In the past, antibiotics were used widely in the industry the composition of the chick microbial populations and
at subtherapeutic levels as growth promoters and as exclude pathogens from colonizing the intestine (144,
prophylactics to minimize the risk of colonization by 146, 147). Exclusion of pathogens is thought to result
enteric pathogens. The relationship between antibiotic from both direct and indirect pathways. Direct effects
use and prevalence/levels of pathogens in poultry pro- include the production of volatile fatty acids, competi-
duction is not clear. Most studies of antibiotic-resistant tion for colonization sites and nutrients, and production
bacteria have focused on the relationship between anti- of bacteriocins by natural microbes; indirect effects in-
biotic use and the emergence, development, and trans- clude stimulation of the host immune system and in-
mission of antibiotic-resistant bacteria. Currently, there creased peristalsis (148). Studies have demonstrated the
is no scientific answer to the following question: Does efficacy of CE in laboratories and field trials (144, 149,

8 ASMscience.org/MicrobiolSpectrum
 Preharvest Food Safety in Broiler Chicken Production

150). However, under commercial conditions, exclusion 4. FDA. 2005. Human health impact of fluoroquinolone resistant Cam-
of pathogens such as Salmonella has been reported to be pylobacter associated with the consumption of chicken, 2001. http://www
.fda.gov/downloads/AnimalVeterinary/SafetyHealth/RecallsWithdrawals
highly variable depending on the organism status in the /UCM152308.pdf.
chick gut and the hatchery environment (80, 151, 152). 5. USDA. 2008. U.S. Department of Agriculture, Food Safety and In-
Various CE products are on the market for use in spection Service. Improvements for poultry slaughter inspection. Appen-
poultry to control Salmonella infection. Due to the dif- dix A. Attribution of human salmonellosis to chicken in the USA.
6. Braden CR. 2006. Salmonella enterica serotype Enteritidis and eggs: a
ference in colonization location of Campylobacter and national epidemic in the United States. Clin Infect Dis 43:512–517.
Salmonella, a different composition of competitive bac- 7. Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ,
teria may be needed to control Campylobacter (153). Griffin PM. 2013. Attribution of foodborne illnesses, hospitalizations, and
According to Schneitz (154), the most effective products deaths to food commodities by using outbreak data, United States, 1998-
2008. Emerg Infect Dis 19:407–415.
are those that contain both large numbers and a diversity
8. Food and Agriculture Organization of the United Nations. 2010.
of bacterial strains. Poultry meat and eggs. http://www.fao.org/docrep/012/al175e/al175e.pdf.
9. USDA. 2012. Progress report on Salmonella and Campylobacter testing
of raw meat and poultry products, CY 1998-2012. http://www.fsis.usda.
CONCLUSIONS gov/wps/portal/fsis/topics/data-collection-and-reports/microbiology/annual
-progress-reports/2012-annual-report.
Foodborne pathogen transmission in preharvest poultry 10. USDA. 2011. FSIS HACCP verification Campylobacter results:
production is complex and therefore requires a com- July-December, 2011. http://www.fsis.usda.gov/wps/portal/fsis/topics
prehensive food safety control and prevention pro- /data-collection-and-reports/microbiology/campylobacter/ct_index.
11. Buzby JC, Farah HA. 2006. Chicken consumption continues longrun
gram to minimize broiler carcass contamination. A wide
rise. Amber Waves 4:5.
range of management strategies and intervention mea- 12. CDC. 2011. Foodborne Diseases Active Surveillance Network
sures exist to control Salmonella and Campylobacter in (FoodNet) 2011 surveillance report. http://www.cdc.gov/foodnet/PDFs
broiler preharvest production. No one single interven- /2011_annual_report_508c.pdf.
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of Salmonella isolates from meat and poultry products: January 1998
to control Salmonella and/or Campylobacter in prehar- through December 2011. http://www.fsis.usda.gov/wps/wcm/connect
vest broiler production. Instead, a collection of measures /26c0911b-b61e-4877-a630-23f314300ef8/salmonella-serotype-annual
that are shown to be effective and cost-effective need to -2011.pdf?MOD=AJPERES.
be applied to control these pathogens. We believe that 14. FDA. 2010. National Antimicrobial Resistance Monitoring System:
Enteric Bacteria (NARMS): 2007 Executive Report. U.S. Department of
vaccination of breeder flocks for Salmonella, strong Health and Human Services, Food and Drug Administration.
biosecurity programs for breeders and broiler flocks, 15. Le Hello S, Hendriksen RS, Doublet B, Fisher I, Nielsen EM,
well-timed feed withdrawal with interventions, and the Whichard JM, Bouchrif B, Fashae K, Granier SA, Jourdan-Da Silva N,
Cloeckaert A, Threlfall EJ, Angulo FJ, Aarestrup FM, Wain J, Weill FX.

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use of feed free of animal by-products are keys to re-
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alized nations, p 163–189. In Nachamkin I, Szymanski CM, Blaser MJ
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