Sources of Salmonella colonization in poultry and pre-harvest controls have been extensively discussed in Parts 1 and 2 of this article series. Part 3 will emphasize processing controls for minimizing the prevalence and/or concentrations of Salmonella in broiler meat. Identified sources for Salmonella colonization of the broilers include: (1) poultry house external environment, (2) poultry feed, (3) hatchery, (4) chicks, (5) poultry house internal environment, (6) water, (7) bird droppings and litter.
Obviously, housing chicks in large numbers results in cross-colonization during grow-out, even if one chick or chicken is colonized. The authors previously discussed that there are no "silver bullets" to eliminate or even minimize the colonization of the chicken gut with Salmonella once the microorganism enters the chicken gut in low numbers. Thus, the processing plant is presented with chickens that have Salmonella in their gastrointestinal tracts at varying levels of prevalence and concentrations within the flock (from the same poultry house) and between the flocks (different houses on the same farm or different farms). Processing plants now have the challenge of addressing these microorganisms and developing strategies to eliminate Salmonella from the chicken's carcass.
Prior to discussing what each unit operation can do and how the risk of Salmonella in finished poultry meat can be reduced, it is important to understand how Salmonella is presented through the bird prior to and during processing. During grow-out, the birds are gradually colonized with Salmonella, and the microorganism is excreted through fecal droppings into the litter. Being coprophagic, the birds consume the contaminated litter, thus spreading Salmonella. While this is the major route of colonization, others include the vectors that introduce the microorganism into the broiler grow-out environment, such as litter beetles, rodents, and flies. Even personnel who work on the farm can become vectors when they move between poultry houses to manage the birds and the environment, if they do not follow strict biosecurity measures.
Poultry processing can be considered to be a collection of processes from the time the birds are caught, placed into the coops, and loaded onto the trailer to the time the meat leaves the processing plant. This article will consider each processing step or unit operation and its implications in terms of food safety or Salmonella prevalence and/or concentrations.
Catching, Loading, Transportation, and Holding
One among the several sequences of events during poultry processing includes the catching, loading, transportation (Figure 1), and holding of the birds, which can collectively be considered as a unit operation rather than a series of operations. This sequence of events has a significant impact on the bird as it is handled, positioned, placed, and exposed to an unfamiliar environment from the time it is caught to the time it is placed on the conveyor at the processing plant prior to being shackled. This results in the birds being exposed to extremes of stress and defecation during the entire process, resulting in cross-contamination with Salmonella, especially on the surface of the birds when presented for processing. A Salmonella incidence is reported of 60 percent on feathers and 46 percent on head and feet, with populations of 3.8 log most probable number (MPN)/sample and 3.1 log MPN/sample, respectively.1 These are relatively high populations of Salmonella presented for processing (in addition to potential contamination from gastrointestinal contents), and subsequent steps should be adequate and targeted to reduce and/or eliminate these Salmonella populations.
FIGURE 1. Birds Being Transported for Slaughter and Processing (Credit: DelmasLehman/iStock/Getty Images Plus via Getty Images)
Unloading, Shackling, Stunning, and Bleeding
The process of placing the birds on the conveyors for subsequent hanging (and the process of hanging itself) presents extreme stress on the birds, which can increase Salmonella shedding by the bird. This increased Salmonella shedding can result in further contamination from other birds, conveyors, hanging personnel (hands that touch the birds), and other contaminated surfaces.
Subsequent to hanging the bird, they are stunned, most often by applying electric current. However, alternative stunning methods are being introduced into poultry processing, including gas stunning, also referred to as "controlled atmosphere stunning (CAS)," where the birds are exposed to atmospheres with low oxygen concentrations. In processing operations where CAS is used, the birds are hung subsequent to the CAS application. The next step, bleeding, is performed mechanically using a rotating blade while the bird neck is presented, to sever the carotid artery and jugular vein. Although there can be a risk of cross-contamination from use of the same blade, without sanitizing between birds, the risk relative to other unit operations may be minimal.
In a majority of poultry processing operations, processors incorporate a series of brushes to remove the organic matter from the surfaces of the birds prior to processing. The application of the brushes may not be consistent from season to season, but may be used heavily during seasons where the caked soil/fecal matter is substantial. The main purpose of these brushes is to remove and significantly reduce the soil or fecal material from the birds entering the scald tank. Minimal reduction in Enterobacteriaceae population (0.3 log CFU/carcass) has been reported subsequent to pre-scald brushes.2
Often, these brushes are also sprayed with either water or chlorinated water to reduce microbial populations. The efficacy of chlorine at this stage, considering the amount of organic matter/soil, may be questionable and is yet to be proven. Although these brushes may serve the purpose of removing extraneous organic material from the surfaces of the birds, they also have the potential for cross-contamination of the birds, specifically with Salmonella in cases where some of the flocks presented for processing have a low prevalence.
Scalding is the process where birds are exposed to warm water to loosen the feather follicles and facilitate feather removal in a subsequent process. Two different types of scalding are adopted by processors—hard and soft. Soft scalding involves maintaining the water temperature between 50 °C and 53 °C. Hard scalding uses a water temperature between 59 °C and 61°C, and the birds are exposed for 1–3 min. Soft scalding preserves the cuticle of the skin and is used for carcasses that are marketed as whole, where the yellowness of the skin color is preferred. However, hard scalding is used in cases where the carcasses are further cut up into parts or deboned and marketed.
Regardless of the scalding method used, these temperatures are not adequate for destroying Salmonella continually brought into the scald tank by the birds on their surface, particularly on the feathers and skin. D values reported for Salmonella in scald water are 23.6 min at 50 °C and 0.2 min at 60 °C. These D values were longer for the microorganism in scald water containing soil (brought in by the birds), with D50°C and D60°C of > 23.6 and 0.4 min, respectively.3 The continual inoculation of Salmonella into the scald tank by the birds being immersed can maintain live Salmonella populations and contaminate any birds from flocks that have low prevalence or populations, resulting in an increase in risk and presenting a greater challenge to subsequent antimicrobial interventions.
Several processors have evaluated the use of chlorine (although this has questionable efficacy due to high organic load) and raising or lowering the pH of the scald water as a means to reduce the risk of Salmonella contamination of the bird surfaces during scalding. However, no conclusive and effective systems have been published to date on these methods, which require further research.
The birds exiting the scalder enter the pickers, a bank of brushes with rubber fingers (different configurations) that use force to remove the feathers from the birds. In most cases, processors utilize a 2-to-3 configuration and in some cases, more pickers are designed for different sections of the bird to remove the feathers. The picking process has gained notoriety for being responsible for driving microorganisms, specifically Salmonella, into the skin either through the force applied on the skin or the process of picking itself, presenting an elegant case of internalization of surface microorganisms into the feather follicles.
Subsequent to scalding, the skin surface is covered with residual liquid from the scalder (often contaminated with Salmonella). When the feathers are removed through the use of picker fingers, the feather follicles are evacuated, and the Salmonella-contaminated water surrounding the follicle is sucked in due to vacuum creation and subsequently sealed by the skin. This process impregnates the skin with Salmonella, which can present significant challenges in terms of reduction and/or elimination of Salmonella populations from the chicken carcasses.
Most processors use chlorinated water either as a drench or a spray on the pickers, but the utility of this is questionable, considering the chlorine concentrations used and also the excessive organic material, which negates the efficacy of the chlorine. The ideal solution to this problem would be to find ways to eliminate Salmonella from the scald water so that the water surrounding the feather follicle is free of the pathogen.
The picking process also applies pressure around the vent area, resulting in the release of cloacal contents onto the carcass. This can further result in contamination of the carcass with the cloacal contents, often containing Salmonella and Campylobacter, thereby increasing the prevalence and concentrations of these microorganisms on the carcass prior to evisceration. One study4 showed that Salmonella prevalence increased from 26.7% to 60% and Campylobacter populations increased from 1.57 log CFU/mL to 3.59 log CFU/mL from pre-pick to post-pick, respectively. Researchers have evaluated using cloacal plugs as a means of minimizing cloacal content leakage and have been successful in preventing contamination of the carcasses.5 However, a more practical solution needs to be developed to ameliorate the risk of leakage of cloacal contents onto the carcass during picking and the resulting contamination of the carcasses with Salmonella and Campylobacter.
Venting, Opening, and Evisceration
Subsequent to picking, the carcasses go through rinsing with either water or water supplemented with antimicrobials, followed by hock removal, and then pass through to the other side of the processing operation for further processes. The next steps include venting, opening, and evisceration—processes of significant consequence to microbial safety of the carcasses. Venting refers to cutting around the vent area to allow removal of the viscera from the carcass. This process is facilitated by a rotating cylindrical saw with teeth that cut around the vent area. The opening step involves a knife that cuts through the skin to allow for the evisceration equipment to remove the viscera from the carcass. While these processes have the potential to cross-contaminate from one carcass to another, the risk is minimal considering other process steps such as evisceration and crop removal.
Subsequent to venting and opening, the carcasses go through automated evisceration equipment, which is designed to scoop the viscera and separate it from the carcass onto the other side or onto a tray for inspection. During this process, the viscera can be cut open due to weak intestinal integrity either resulting from extended feed withdrawal or faulty equipment. When this happens, the gut contents can contaminate the equipment and result in persistent and continual cross-contamination of subsequent carcasses that are processed. While the evisceration equipment is continually sprayed with chlorinated water, the efficacy of such sprays in reducing populations of Salmonella on the equipment surface is questionable.
The function of the crop in a bird is to temporarily store the ingested feed. During the time the feed is in the crop, it may undergo some softening due to enzymatic activity by the enzymes in the feed (exogenous and endogenous), as well as by microbial enzymes. While it is possible that the microbial population can be dominated by lactobacilli, evidence of the antimicrobial activity against Salmonella by these lactobacilli is limited. The residence time of the feed in the crop varies significantly, from 7–25 minutes in broilers when provided feed ad libitum with 24 hours of light per day.6
During feed withdrawal, the birds may gorge themselves with litter, which can be a significant source of Salmonella and other enteric pathogens. Salmonella incidence was reported to increase significantly, from 1.9 percent before feed removal to 10 percent after feed withdrawal.7 The crop contents can provide optimal conditions for survival and potential growth of Salmonella, and can contaminate the equipment if the crop is ruptured during the crop removal process. Crop removal is achieved by rotating a serrated probe that goes through the neck area; the crop is removed by brushes when it is extended. Subsequent to removal of the crop, the probe is retracted, and the carcass goes on to the next unit operation.
Subsequent to crop removal, the necks are removed from the carcass with knives, followed by other unit operations. To date, no reports suggest that this step poses any risk in terms of microbial cross-contamination.
On-Line Reprocessing, Inside-Outside Bird Washing, and Chilling
The next steps constitute the majority of those designed for Salmonella risk reduction in poultry processing. In on-line reprocessing, the carcasses are sprayed or drenched with high volumes of water containing antimicrobials, such as chlorine or peroxyacetic acid (PAA). Several other antimicrobials are approved for use during on-line reprocessing and can be accessed from the U.S. Department of Agriculture Food Safety and Inspection Service's (USDA FSIS') "List of Approved On-Line Reprocessing (OLR) Antimicrobial Systems for Poultry."8 The system is designed to remove any visible fecal or ingesta contamination from chicken carcasses in lieu of manual carcass washing and/or trimming. The inclusion of antimicrobials also achieves the dual purpose of reducing microbial populations, including those of Salmonella.
The primary purpose of inside-outside bird washing (IOBW) is to remove any residual fecal or ingesta material from the carcasses entering the chiller, in order to meet USDA FSIS' zero-tolerance policy on visible fecal or ingesta. The efficacy of IOBW in reducing Salmonella populations is debatable, as the residence time at the IOBW for the carcasses is minimal and the spray application of antimicrobials for skin-on chicken products has not been shown to be effective in reducing microbial populations.9
Carcass chilling is typically considered a single-unit operation, but is applied as several steps in processing operations with several combinations of (1) pre-chiller, (2) main chiller, (3) post-chill dip, and (4) potentially another step prior to the pre-chiller. While the main objective of these chillers is to chill the chicken carcass to temperatures that will inhibit microbial growth, the requirement of a critical control point during processing, as required by the Pathogen Reduction: Hazard Analysis and Critical Control rule, has resulted in several processors incorporating antimicrobials into the chiller water. Initially, chlorine was used as the antimicrobial; more recently, PAA has become the antimicrobial of choice for most processors. PAA has several advantages in that it is equally effective at low temperatures used in poultry chilling operations, its efficacy is not affected by the presence of organic matter, it is effective at a wide pH range, and pH values above pKa do not seem to affect its antimicrobial efficacy.
Today, chilling operations are considered as a main antimicrobial intervention where the majority of the reduction in Salmonella population or prevalence occurs. Based on the configuration of the chilling operations (e.g., types such as paddle, screw, swing, etc.; numbers; temperatures; and pH values), the efficacy of these operations can vary. An overall Salmonella incidence of 71.8 percent at rehang was reported, while only 20.2 percent were positive post-chill, indicating the efficacy of the chillers in reducing Salmonella incidence in a study conducted across major poultry integrators and 20 poultry processing operations.10 It should also be noted that this study was conducted when the majority of the poultry processors were using chlorine in the chillers. We know that PAA is a more effective antimicrobial and can be easily managed compared to chlorine, which is dependent on the solution pH and the organic load, although processors have used available free chlorine as the criterion.
A recent study reported Salmonella incidence of 94 percent at live receiving, 4 percent pre-chill (rehang), and 0 percent post-chill on poultry carcasses sampled at a processing facility.11 It would be interesting to conduct an extensive study to further evaluate Salmonella incidence across the industry (and include more processing plants) today, with PAA as the choice antimicrobial at the chilling stage compared to chlorine, as reported in a 2009 study.12
It is interesting to note that the 2002 study11 reported 0 percent Salmonella prevalence post-chill, but that it had increased to 10 percent after cut-up, where the wings were sampled (the majority of the chicken wing surface is covered with skin). This increase in Salmonella prevalence can be attributed to either cross-contamination during further processing (cut-up) or the natural prevalence of Salmonella embedded into the skin during the picking process, as discussed previously.
Similarly, a 2014 study13 reported Salmonella prevalence of 5 percent, 5 percent, and 48 percent using the neck skin excision, whole carcass rinse, and whole carcass enrichment methods, respectively, from naturally contaminated chicken carcasses obtained from commercial processing operations. The neck skin excision method and the whole carcass rinse methods are the methods of choice in the EU and U.S., respectively. The higher Salmonella prevalence observed using the whole carcass enrichment method can be attributed to the inability of the carcass rinse method to extract all of the Salmonella cells from the carcass, as the method can remove only surface microbial cells into the rinse and not those embedded in the feather follicles. Furthermore, of the 400 mL of the total buffer solution used for sampling, only 35 mL is used for the enrichment step within the Salmonella detection method, another step where bias toward lower prevalence is introduced. Regardless, the apparent efficacy of the chillers as antimicrobial interventions may be amplified, and the true prevalence should be considered when making decisions on reducing Salmonella risk from poultry meat.
As discussed earlier, USDA FSIS data indicates an increase in the prevalence of Salmonella from carcasses (collected after the carcass chilling step) and carcass parts. This is demonstrated in the 2022 study,11 where the Salmonella prevalence in chicken wing samples (10 percent) was greater than the carcass samples (0 percent). It would be interesting to evaluate the Salmonella prevalence on the wings or other cut-up parts under controlled conditions, without the confounding effect of potential cross-contamination during commercial processing.
During the step where cut-up parts are treated with antimicrobials such as PAA, using a dip or spray system, there is a similar potential to reduce Salmonella populations on the surfaces of carcass parts as in other, subsequent processing steps. However, the ability to do the same for Salmonella cells embedded in the carcass/parts skin during these steps is questionable.
The contemporary poultry processing system was designed a number of decades ago, when the threat of foodborne pathogens was not as significant or as well understood. It is known that the birds presented for processing have Salmonella on their surfaces (feathers, skin, feet, etc.), as well as in the gastrointestinal tract. The initial unit operations of pre-scald brushes, scalding, and picking result in cross-contamination of all the birds and, more importantly, the embedding of Salmonella cells into the skin of the bird, making it impossible to reduce and/or eliminate the microorganism at subsequent processing steps—including the antimicrobial interventions designed to achieve this purpose. Antimicrobial interventions, primarily the chilling unit operations (regardless of the number of stages and PAA parameters) can only reduce and/or eliminate Salmonella surface contamination and not the cells embedded into the skin.
It is possible that during the venting, evisceration, and crop removal unit operations, contamination of processing equipment can occur. Mechanisms to sanitize the equipment subsequent to such contamination from the gastrointestinal contents are lacking, resulting in potential cross-contamination of other carcasses. At present, poultry processing unit operations are not designed to operate under adequate sanitary conditions to prevent cross-contamination from the gastric contents of the bird carcasses.
Evidence continues to build that incorporating additional antimicrobial interventions with PAA or other antimicrobials at processing may achieve only marginal reductions in Salmonella populations and/or prevalence. Thus, a significant reduction in the risk of Salmonella from poultry meat at processing requires reevaluation of the unit operations to address Salmonella from bird surfaces and subsequent embedding of the microorganism into the skin, as well as cross-contamination resulting from contaminated equipment due to breakage and/or leakage of the gut.
Further reductions in Salmonella risk can be achieved only through persistent efforts to reduce and/or eliminate the sources of the microorganism at the grow-out stage and Salmonella colonization of the flock during grow-out. The effectiveness of processing controls is reliant on a reduction in Salmonella populations on bird surfaces and in the gastrointestinal contents, emphasizing the need to exercise control during the production stage.
- Cason, J. A., A. Hinton Jr., J. K. Northcutt, R. J. Buhr, K. D. Ingram, D. P. Smith, and N. A. Cox. "Partitioning of external and internal bacteria carried by broiler chickens before processing." Journal of Food Protection 70 (2007): 2056–2062.
- Pacholewicz, E., L. J. Lipman, A. Swart, A. H. Havelaar, and W. J. Heemskerk. "Pre-scald brushing for removal of solids and associated broiler carcass bacterial contamination." Poultry Science 95 (2016): 2979–2985.
- Yang, H., Y. Li, and M. G. Johnson. "Survival and death of Salmonella Typhimurium and Campylobacter jejuni in processing water and on chicken skin during poultry scalding and chilling." Journal of Food Protection 64 (2001): 770–776.
- Berrang, M. E., W. R. Windham, and R. J. Meinersmann. "Campylobacter, Salmonella, and Escherichia coli on broiler carcasses subjected to a high pH scald and low pH postpick chlorine dip." Poultry Science 90 (2011): 896–900.
- Musgrove, M. T., J. A. Cason, D. L. Fletcher, N. J. Stern, N. A. Cox, and J. S. Bailey. "Effect of cloacal plugging on microbial recovery from partially processed broilers." Poultry Science 76 (1997): 530–533.
- Classen, H. L., J. Apajalahti, B. Svihus, and M. Choct. "The role of the crop in poultry production." World's Poultry Science Journal 72 (2016): 459–472.
- Corrier, D. E., J. A. Byrd, B. M. Hargis, M. E. Hume, R. H. Bailey, and L. H. Stanker. "Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed withdrawal." Poultry Science 78 (1999): 45–49.
- U.S. Department of Agriculture, Food Safety and Inspection Service. List of Approved On-Line Reprocessing (OLR) Antimicrobial Systems for Poultry. October 2022. https://www.fsis.usda.gov/sites/default/files/media_file/2021-09/7120.1-olr-oflr-tables.pdf.
- Smith, D. P., J. K. Northcutt, and M. T. Musgrove. "Microbiology of contaminated or visibly clean broiler carcasses processed with an inside-outside bird washer." International Journal of Poultry Science 4 (2005): 955–958.
- Bailey, J. S., N. J. Stern, P. Fedorka-Cray, S. E. Craven, N. A. Cox, D. E. Cosby, S. Ladely, and M. T. Musgrove. "Sources and movement of Salmonella through integrated poultry operations: A multistate epidemiological investigation." Journal of Food Protection 64, no. 11 (2001): 1690–1697. https://meridian.allenpress.com/jfp/article/64/11/1690/168171/Sources-and-Movement-of-Salmonella-through.
- De Villena, J. F., D. A. Vargas, R. Bueno López, D. R. Chávez-Velado, D. E. Casas, R. L. Jiménez, and M. X. Sanchez-Plata. "Bio-mapping indicators and pathogen loads in a commercial broiler processing facility operating with high and low antimicrobial intervention levels." Foods 11 (2022): 775.
- Berrang, M. E., J. S. Bailey, S. F. Altekruse, W. K. Shaw Jr., B. L. Patel, R. J. Meinersmann, and P. J. Fedorka-Cray. "Prevalence, serotype, and antimicrobial resistance of Salmonella on broiler carcasses postpick and postchill in 20 U.S. processing plants." Journal of Food Protection 72 (2009): 1610–1615.
- Cox, N. A., R. J. Buhr, D. P. Smith, J. A. Cason, L. Rigsby, D. V. Bourassa, P. J. Fedorka-Cray, and D. E. Cosby. "Sampling naturally contaminated broiler carcasses for Salmonella by three different methods." Journal of Food Protection 77, no. 3 (2014): 493–495. https://meridian.allenpress.com/jfp/article/77/3/493/197239/Sampling-Naturally-Contaminated-Broiler-Carcasses.
Harshavardhan Thippareddi, Ph.D., is the John Bekkers Professor of Poultry Science in the Department of Poultry Science at the University of Georgia in Athens, Georgia.
Manpreet Singh, Ph.D., is Professor and Head of the Department of Food Science and Technology at the University of Georgia in Athens, Georgia.