The control of Salmonella in chicken processing plants is an ongoing challenge for many factories around the globe


Poultry largely outnumbers humans with approximately one person for every three birds [1]. Meat and eggs produced from poultry are consumed across numerous cultures and are among the most efficient forms of protein [1,2].

In 2016, the global livestock environmental assessment model (GLEAM) generated by the Food and Agriculture Organization of the United Nations [3] approximated egg production to be 73 million tons and meat production to be 100 million tons. These numbers are constantly increasing due to population growth, escalating incomes and urbanization [1,4,5].

Demand for poultry is increasing not only in developing countries but also developed countries [5,6]. The demand is met because chickens are intensively produced; chickens rapidly reach a sufficient size and are then slaughtered and processed through highly automated systems that allow for rapid throughputs [6].

The shift from free range farming towards intensive practices has allowed for tremendous growth in the supply of poultry as a protein source [6].

Intensive practices have utilized various breeding techniques, feed manipulation and antibiotic administration to optimize size, growth, and desirable attributes [1,7].

Animal sourced protein provides various micronutrients [2] that are challenging to acquire in sufficient quantities from plant based protein, such as vitamins A and B, zinc, iron, and calcium [1]. Poultry, specifically, is cheap, a high quality source of protein and has very few negative associations with religious beliefs, and is therefore often the animal protein of choice in developing countries [1,8].

In a study conducted by Zeng et al. [9], where trends in meat consumption were tracked and analyzed in American adults from 1999 to 2016, it was found that chicken consumption increased from approximately 250 g per week in 2000, to 300 g per week in 2016. Conversely, the consumption of turkey remained relatively constant. Furthermore, in Kuwait, average poultry meat consumption per capita from 2004 to 2016 was a whopping 64.4 kg/year (approximately 1.2 kg/week) [10].

Another country showing substantial growth is Brazil; Brazil is the country with the largest export rate of poultry meat and the second highest poultry meat producer globally, making it a top competitor with China and the US [11].

This increased preference and, consequently, production could be due to a couple of factors: firstly, because the price of red meat has increased while the price of chicken has remained constant, and secondly, many health concerns have been associated with red meat which, thus, have created the perception of chicken being a healthier and leaner option [9,12].

Another trend which is affecting the supply of poultry is ready to eat (RTE) meals. This includes snack foods, take away meals and dining out. This manner of consumption is becoming more popular and is seen as more convenient than preparing a meal in the home [6,13].

With this increasing demand, there are many consumers that are becoming increasingly aware of quality and are now purchasing products with the consideration of food safety, environmental impact, and animal welfare [6,14]. This forces the industry to keep up with the increasing sophistication and refining of food technology [14].

The poultry industry on a global scale is significantly influenced by these four areas of pressure in society, namely, food security, the economy, environmental impact and food safety [1]. These four dimensions are responsible for the delicate balance that the poultry industry continuously struggles to satisfy with the rapidly increasing demand.

Today, food poisoning sickens roughly 1 in 6 Americans every year, according to the CDC, and salmonella hospitalizes and kills more people than any other foodborne pathogen. Each year, about 1.35 million people get sick from salmonella. While most recover, more than 400 people die and 26,500 people are hospitalized. Some are left with long-term conditions like severe arthritis and irritable bowel syndrome. Salmonella costs the economy an estimated $4.1 billion a year, more than any other type of food poisoning.

Salmonella outbreaks have been linked to other foods like onions, but poultry remains the biggest culprit, and people are eating more of it than ever. On average, people in the U.S. eat nearly 100 pounds of chicken each year, a number that has grown by about 40% in the last 25 years.

Cooking poultry to an internal temperature of 165 degrees will kill salmonella. But studies by the USDA and others have found that despite decades of consumer education, home cooks routinely cross-contaminate their kitchens, and few use a meat thermometer to ensure their poultry is cooked properly.

Illnesses haven’t declined even as salmonella rates in raw poultry have. And infections are getting harder to treat. The CDC recently found that salmonella infections were becoming increasingly resistant to antibiotics. In contrast, food poisoning related to E. coli O157:H7 has dropped by about 70%.

Consumer advocates, industry consultants and former USDA officials say that’s because the agency focuses solely on whether salmonella is found in chicken or turkey at the processing plant.

This approach has been criticized for years. One former meatpacking executive called it “worthless.” Even the USDA’s own research arm has said the agency’s measure for salmonella is “not a good indicator” of food safety.

The USDA doesn’t consider two key risk factors: how much salmonella is in the poultry and how dangerous that type of salmonella is. There are 2,500 types of salmonella, but only a fraction cause the vast majority of illnesses.

The industry has greatly reduced the prevalence of one common type of the bacteria, known as salmonella Kentucky, which rarely causes illnesses in the U.S. But it’s made far less progress with the types of salmonella most likely to make people sick, the ProPublica analysis found.

The rate of infantis, for example, has more than quintupled over the past six years.

The full extent of the salmonella problem isn’t even known. The agency does little testing for salmonella to begin with. On an average day in 2020, the USDA took about 80 samples of raw poultry across hundreds of processing plants. But those plants slaughter more than 25 million chickens and turkeys a day.

In recent years, consumer advocates have recommended the agency ban the sale of raw meat carrying the types of salmonella that most often make people sick. That approach has contributed to improvements in Europe. In the U.S., the FDA has seen a dramatic decrease in salmonella outbreaks tied to eggs since the 1990s when it began targeting the most common type.

Last month, a few of the largest poultry companies, including Perdue and Tyson, joined with the CSPI and other consumer advocates to urge the USDA to fix the system. But the letter to the agency didn’t outline specific reforms, and a consensus on salmonella regulations has long proved elusive.

The last push came during the Obama administration, but citing the need for more data, the USDA rejected a proposal to ban certain antibiotic-resistant strains. The agriculture secretary at the time was Tom Vilsack, who now leads the agency again under President Joe Biden.

As the food safety project director for the Pew Charitable Trusts before joining the USDA, Eskin also pushed for reform, but her efforts were met with resistance. With food safety directors from some of the largest companies, she helped craft recommendations to Congress to modernize the meat safety system, including setting new limits on salmonella contamination and giving regulators oversight of farms.

The group sought to enlist trade associations, which represent not only the biggest players but hundreds of other companies. But when it comes to regulation, divergent interests often leave the trade groups lobbying for the lowest common denominator. “They shut us down,” she said in an interview before taking her government post. “They’re the ones that blocked us — not the companies, the trade associations.”

Asked what was standing in the way of change, she said, “I’ll make it simple: Powerful interests in the industry do not want it.”


As previously mentioned, foodborne outbreaks pose many risks, both in terms of health and economic loss. The pathogen of particular emphasis and concern in poultry is Salmonella [32,33,34]. The United States, alone, spends approximately 11.588 billion dollars on collateral damage and improving prevention methods for Salmonella infections originating from poultry products annually, while the EU’s estimated costs are more than €3 billion a year [33,35].

Salmonella has been pinpointed as the source of many cases of food poisoning as well other severe health defects over the last century [32,36]. The continual outbreaks due to Salmonella make this resilient genus and its characteristics a focused point of research for many health and science professionals despite an existing abundance of information [33].

The survival of Salmonella can be accredited to its resistance-development rates being more rapid than that of other pathogenic bacteria placed under the same preventative pressures [36,37]. Managing an organism that is changing incessantly requires an in depth understanding of its characteristics and what the outward expression from these characteristics may imply upon human consumption [32].

General Characteristics

The genus of Salmonella, under the family of Enterobacteriaceae, are rod-shaped (approximately 2 μm in size), motile (due to presence of peritrichous flagella), glucose-fermenting, Gram-negative, facultative anaerobes that do not form spores [38,39,40].

Salmonella can commonly be found on dairy products, meat products (especially raw poultry) and fresh produce [36]. The various parameters and conditions in which Salmonella can survive are given in Table 3. As Salmonella is not a spore-former, it can be destroyed easily with heat, particularly in food products with high water activities [32].

Forysthe [34] tells us that a temperature–time combination of 15–20 min at 60 °C should be sufficient to ensure the death of all Salmonella present in the food product, and Bell and Kyriakides [41] also assure us that growth of most serotypes of Salmonella will be inhibited below 7 °C and a pH of 4.5.

Table 3

Parameters for survival and growth of Salmonella (adapted from [34,41]).

ParameterApproximate Growth Range
Temperature5–46 °C (optimum = 38 °C)
Water activity0.94–0.99

Salmonella Serovars

The Salmonella genus is further divided into two species, namely, Salmonella enterica (S. enterica) and S. bongori [42]. Serovars of Salmonella can be grouped by their O (somatic), Vi and H (flagellar) antigen combination; O antigens being lipopolysaccharides of the outer membrane, Vi antigens being the sugar composition on the capsid, and the H antigens being the sugar combination found on the flagella [43].

This method of identification is responsible for the quarter of a million serovars widely recognized so far, with the majority of the serovars from S. enterica, a number that is increasing annually [42]. Furthermore, serovars can also be identified using phage sensitivity testing, whereby the Salmonella is treated with specific, known bacteriophages and the resulting lytic activity reveals which serotype of Salmonella is present due to the range of host specificity of the bacteriophage [44].

The system of identifying and categorizing Salmonella can be confusing due to more than 250,000 known serovars [40,43], Forsythe [34] simplifies this, and, rather, emphasizes the importance of three different types of Salmonella with regards to human health: non-typhoid Salmonella, Salmonella typhi (S. typhi) and Salmonella paratyphi (S. paratyphi).

Non-typhoid Salmonella is distinguished by an incubation period of 6–72 h after consumption, causing symptoms such as diarrhea, blood in the stools, consequent dehydration, fever, vomiting, weakness, and abdominal pain [40]. Conversely, S. typhi and S. paratyphi have an incubation period of 1–4 weeks, causing symptoms that are like typhoid, such as headaches, fever, body weakness and aches, constipation, or diarrhea [34].

Various food properties influence the infectious dose of different serotypes of Salmonella. For example, in foods that have a higher fat content, the bacterial cells are protected and thus fewer than 100 cells may cause illness [41].

Thus, a standard level of detection in RTE foods had to be established that ensured that food safety would be maintained despite the serotype. Thus, it was determined that there should be less than one cell of Salmonella per 25 g of a RTE food sample [45].

Treatment of Salmonella in the Slaughter Setting

Despite stringent measures and efforts in rearing chickens in a way that seeks to eliminate Salmonella from the hatchery level—such as good hygiene practices, isolating infected flocks and the use of specialized feed—the safe passage of poultry from farm to fork remains under scrutiny due to contaminated poultry meat continuously having the largest negative impact on public health.

Thus, it is important that the processors of poultry meat utilize existing, new, or additional measures to assist in the prevention of Salmonella [46,47,48]. In the United States, poultry processing facilities have had to employ a criterion established by the United States Department of Agriculture’s Food Safety and Inspection Service (USDA-FSIS) whereby for every 51 samples collected, less than 7.5% of them should be Salmonella positive [49].

Some of the measures employed by poultry processors include a postchilling immersion tank with various antimicrobials as well as spray applications, also with various antimicrobials. The combination of these methods/addition of these methods to existing preventative measures create a “hurdle concept” in the processing plant for the elimination of Salmonella [47,48]. Some of these antimicrobials and their respective applications can be seen in Table 4.

Table 4

Some of the widely used safe and suitable antimicrobials stipulated for use in poultry processing to produce raw poultry meat products in the United States (data from [50]).

Aqueous sulfuric acid/sodium sulfateWash, spray or immersion dip on surface of poultry productsConcentration that employs pH of 1–2.2 of poultry
Measured on the meat surface
Acidified sodium chloritePoultry pieces and carcasses500–1200 ppm. May be used in a mixture with any “generally recognized as safe” (GRAS) acid to obtain pH 2.3–2.9
Poultry carcasses, pieces, organs and trimmingsMay be added to a GRAS acid to obtain pH 2.2–3
May be further diluted with basic sodium bicarbonate to obtain pH 5–7.5
Use in a dip/spray, should not have sodium chlorite concentration >1200 mg/kg or chlorine dioxide concentration >30 mg/kg
Use in a prechilling or chilling solution for carcasses, sodium chlorite should be 50–150 ppm
Contact time is not detrimental as long as temperature is 0–15 °C
Bacteriophage solution (Salmonella specific)Applied to feathers of live poultry preslaughterSpray or fine mist application, or wash
Calcium hypochloriteUsed on eviscerated or whole chicken carcassSpray application should not have free available chlorine >50 ppm
Water used for poultry processing and for chiller waterFree available chlorine should not be >50 ppm for inlet water
Measure at potable water inlet
Water recirculated from chiller via heat exchangersFree available chlorine should not be >5 ppm at inlet to chiller
Retreating carcasses that are contaminatedFree available chlorine should be 20–50 ppm
GibletsFree available chlorine should not be >50 ppm at inlet to chiller
Chlorine gasUsed on carcass that is whole or has been evisceratedSpray application where free available chlorine should not >5 ppm
Measured before application
Used in water of chillerFree available chlorine should not >50 ppm
Should be measured at inlet of potable water
Water recirculated from chiller via heat exchangersFree available chlorine should not >5 ppm
Measured at chiller inlet
Retreating carcasses that are contaminatedFree available chlorine should be 20–50 ppm
GibletsFree available chlorine should not >50 ppm.
Measured at inlet to chiller
Chlorine dioxideWater used for processing of poultryResidual chlorine dioxide should not >3 ppm
DBDMH (1,3-dibromo-5,5- dimethylhydantoin)Used in water of chiller and water of inside–outside bird washer (IOBW). In addition, used for processing of poultry carcasses, organs and pieces.Active bromine should not be >100 ppm
Added to water for ice making which is then used in processing of poultryActive bromine should not >100 ppm (or max 90 mg DBDMH per kg water)
Hypochlorous acidUsed on carcass that is whole or has been evisceratedFor spray application, free available chlorine should not >50 ppm
Measured before application
Added to water used for processing of poultryFree available chlorine should not >50 ppm
Used in water for chillerFree available chlorine should not >50 ppm
Measured at inlet of potable water
Water recirculated from chiller via heat exchangersFree available chlorine should not >5 ppm
Measure at chiller inlet
Used for re-treating poultry carcasses that are contaminatedFree available chlorine should be 20–50 ppm
GibletsFree available chlorine should not >50 ppm
Citric and Hydrochloric acid solution (pH 1–2)Poultry carcasses, pieces, organs and trimmingsSpray or dip application with 2–5 s contact time
Measure before application
1.87% citric acid, 1.72% phosphoric acid and 0.8% hydrochloric acid solutionPoultry carcassesSpray application with 1–2 s contact time. Should run off carcasses for 30 s
Lactic acidPoultry carcasses, pieces, organs and trimmings5% concentration for post chilling
Peroxyacetic acid (PAA), hydrogen peroxide (HP), acetic acid (AA), and 1 hydroxyethylidene-1, 1 diphosphonic acid (HEDP) solutionUsed in water for poultry processing, scalding tanks, ice production and spray applicationsPAA should not >220 ppm, HP should not >110 ppm, HEDP should not >13 ppm
PAA, octanoic acid (OA), Peroxyoactanoic acid (POA) HP, AA, HEDP solutionCarcasses, pieces, trimmings and organsPAA should not >220 ppm, HP should not >110 ppm, HEDP should not >13 ppm
PAA, HP, HEDP solutionAdded to water for processing of carcasses and pieces. Applied via spray, dip, wash or added to chiller or scalding tank.PAA should not >2000 ppm and HEDP should not >136 ppm
PAA, HP, AA, HEDP solutionUsed in water or ice for applied on whole carcasses, pieces, trimmings and organs. Applied via spray, dip, wash or added into chiller or scalding tank waterPAA should not >220 ppm, HP should not >80 ppm, HEDP should not exceed 1.5 ppm
Added to process water for application to carcasses, pieces, trimmings and organs via spray application, dip, rinse, wash or added into chiller or scalding tank waterPAA should not >2020 ppm, HP should not exceed 160 ppm, HEDP should not exceed 11 ppm
Sodium hypochloriteApplied to eviscerated or whole carcassesFor spray application, free available chlorine should not >50 ppm
Added to water for processing of poultryFree available chlorine should not >50 ppm at potable water inlet
Added to water in chillershould not >50 ppm
Added to water recirculated from chiller via heat exchangersFree available chlorine should not >5 ppm at inlet to chiller
Retreatment of contaminated carcassesFree available chlorine should be 20–50 ppm
GibletsFree available chlorine should be 20–50 ppm


Antibiotic resistance has compromised the effectiveness of antibiotics as a treatment against infections [81,82]. Antibiotic resistance is caused by the misuse of antibiotics in the treatment of an illness; this results in the targeted bacteria no longer being sensitive to the antibiotic for which it was created [83].

In the US, an annual estimate of approximately 23 × 106 kg of antibiotics are used, of which 50% are administered to humans while the other 50% are used for livestock in disease prevention/treatment [82]. Due to the rising numbers of organisms resistant to antibiotics, it is essential that more than one treatment should be available for various illnesses to avoid a situation like that before the existence of antibiotics, when there was a high death rate due to common infections [83].

Antimicrobial resistance is also on the rise where surface and cleaning antimicrobials are no longer able to eliminate the bacteria of concern, thus, we face a large scale resistance problem which requires urgent attention and alternatives, and a possible solution is bacteriophages [81,82,84].

The discovery of the bacteriophage phenomenon is largely debatable: Ernest Hankin in 1896 “first” suggested that there was an invisible, inexplicable antibacterial activity of Vibrio cholerae that he noticed in the rivers of India [85,86]. He further suggested that whatever was responsible for this antibacterial activity was small enough to pass through porcelain filters [85]. Eventually, Frederick Twort, some 20 years later, suggested that Hankin’s findings could have been a virus, and, finally, two years after this, Felix d’Herelle “officially” classified this virus as a bacteriophage [87,88].

Phages naturally exist in abundance all around us: in fresh water it is suggested that there are approximately 109 phages/mL while marine environments may have up to 107 phages/mL [89]. Fermented foods, fresh vegetables, topsoil and even delicatessen foods have been found to be good sources of phages too, meaning that humans are constantly exposed to—or are consuming—phages [89].

Bacteriophages (phages) are known as predators of bacteria; phages are essentially viruses which infect and subsequently cause bacterial cell death. Phages attach themselves to specific receptor sites on the bacterial cell wall, meaning that phages will only infect a specific range of bacteria while any other present cells or organisms will be unaffected [90,91].

Hence why phage consumption by humans has no adverse effects and can be given the GRAS status [89,91]. After attachment to the bacterial cell wall, the phage injects its genetic material into the bacterial host which causes the genes of the phage to be expressed and ultimately causes the bacterial cell to die [92].

Depending on whether the bacteriophage is virulent or temperate, one of two events may occur after bacterial cell infection [89,90].

Virulent phages (also known as strictly lytic) are phages that cannot incorporate their genetic material into the bacterial chromosome to create lysogens, this means that after infection, virulent phages will always initiate replication within the host, progeny and then lysis (cell death) of the bacterial cell [89,92,93].

Temperate phages (also known as lysogenic), on the other hand, may cause progeny but not kill the bacterial host cell or may integrate some of the phage genetic material into that of the hosts. This results in the replication of the bacterial DNA along with the phage DNA which may result in modifications of the host characteristics, which could lead to host resistance. Alternatively, phage genomes introduced into that of the bacterial genomes may undergo recombination and lead to undesirable changes in the phage genome [94,95,96].

Thus, it is preferable to use phages that are virulent (lytic), rather than temperate, for phage therapy because destruction of the bacterial host is rapid and there is minimal chance of interactions with the host genome [94,96,97].

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