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1 Introduction

Contamination of beef carcass surfaces with Escherichia coli O157:H7 and Salmonella occur during the slaughter process due to contact with feces and the hide which are the most likely sources of contamination (Kochevar et al. 1997; Phebus et al. 1997; Huffman 2002; Keeton and Eddy 2004; Edwards and Fung 2006). Similarly, various processing steps have been reported to contribute to contamination or cross-contamination of the poultry carcasses including live receiving, immobilization, bleeding, scalding, feather removal, evisceration, and chilling (U.S. Department of Agriculture 2008a, b). To reduce the risk of foodborne diseases related to meat and poultry, the United States Department of Agriculture’s Food Safety Inspection Service (USDA-FSIS) issued the Pathogen Reduction: Hazard Analysis and Critical Control Point (PR/HACCP) regulation on July 25, 1996. PR/HACCP established pathogen reduction requirements applicable to meat and poultry establishments to reduce the occurrence and numbers of pathogens in meat and poultry products (U.S. Department of Agriculture 1996; Mead et al. 1999). However, an estimated 9.4 million episodes of foodborne illnesses, 55,961 hospitalizations, and 1,351 deaths have been attributed to 31 major pathogens in the USA each year. Norovirus caused the most of illnesses (58 %) followed by nontyphoidal Salmonella spp. (11 %), Clostridium perfringens (10 %), and Campylobacter spp. (9 %). Nontyphoidal Salmonella spp. (35 %), norovirus (26 %), Campylobacter spp. (15 %), and Toxoplasma gondii (8 %) were the leading causes of hospitalization. Nontyphoidal Salmonella spp. (28 %), T. gondii (24 %), Listeria monocytogenes (19 %), and norovirus (11 %) were the leading causes of death (Scallan et al. 2011). In response to demands from consumers for safer meat and poultry products and implementation of government regulations, numerous studies testing possible interventions have been conducted by the industry and researchers including physical and chemical decontamination treatments.

2 Physical Decontamination Treatments

A variety of thermal and nonthermal decontamination systems are currently available for physical decontamination of carcasses. Physical decontamination treatments are designed to reduce or eliminate the numbers of microorganisms on the carcasses by destroying (thermal or nonthermal methods) or removing pathogens (e.g., by washing or spraying). Some of these physical systems include water-based treatments for instance washing, spray-washing, hot water pasteurization, stem pasteurization, and steam-vacuuming. Others may include carcass trimming, irradiation, and HPP systems.

2.1 Water-Based Treatments

Washing is a fundamental unit operation in the processing of meat and poultry and mainly used to remove visible contaminants such as soil, feathers, and other debris and fecal contamination from the surface of the carcasses. However, water wash as a single carcass intervention has been reported to slightly reduce the bacterial load on the carcasses (Hardin et al. 1995; Castillo et al. 1998a; Northcutt et al. 2003b, 2005; Smith et al. 2005, 2007). The removal of the contaminants by washing with water could be increased using a rinse, spray, and immersion bath or steam treatment.

In commercial poultry processing, spraying or some form of rinsing is used for carcass washing at pressures sufficient enough to remove visible contamination, usually in a whole carcass inside–outside washer. Furthermore, washing might include multiple sprays of water from bleeding through chilling contributing to the reduction of Salmonella prevalence on carcasses by 50–90 % (Bolder 2007; Buncic and Sofos 2012). Loretz et al. (2010) indicated that cold and warm water treatments including immersion chilling reduced Salmonella by 0.6–1.3 log units. Similarly, inside–outside cabinet washer has been reported to slightly reduce aerobic plate counts, as well as Salmonella, Campylobacter, Escherichia coli, and coliforms (Fletcher and Craig 1997; Byrd et al. 2002; Jimenez et al. 2002, 2003; Li et al. 2002; Northcutt et al. 2003b, 2005; Smith et al. 2005, 2007). Benli et al. (2011) also reported only a 0.3 log CFU/ml reduction in Salmonella following water spray of inoculated poultry carcasses. Likewise, spray washing poultry carcasses with water alone has been reported ineffective for reducing either Salmonella or the total bacterial load on carcasses in several studies (Hwang and Beuchat 1995; Li et al. 1997; Sakhare et al. 1999; Northcutt et al. 2003b, 2005; Mehyar et al. 2005). Furthermore, Lillard (1988) proposed that water immersion of poultry carcasses during processing forms crevices on the skin in which bacteria lodge and are protected from effects of saline and other solutions of varying ionic strength or surfactants. This hypothesis was suggested to explain the persistence of salmonellae on poultry carcasses and the ineffectiveness of some antimicrobial applications for reducing salmonellae. However, Morrison and Fleet (1985) reported that immersion treatment of inoculated chicken carcasses with hot water (60 °C) for 10 min reduced Salmonella Typhimurium by 2 logs. Conversely, Berrang et al. (2000) found that a second scald applied after defeathering either as an immersion treatment at 60 °C (28 s immediately or 30 min after defeathering) or as a spray treatment at 71–73 °C (20 s immediately or 30 min after defeathering) was not effective for reducing Campylobacter, E. coli, and coliforms on chicken carcasses. Sanchez et al. (2002) compared immersion chilling and air chilling for reducing microbiological load, the incidence of Salmonella spp. and Campylobacter spp. on broiler carcasses. They found no significant differences between immersion chilling and air chilling for total aerobic counts (3.38 log and 3.31 log CFU/ml, respectively), generic E. coli (1.17 log and 1.43 log CFU/ml, respectively), or coliforms (1.72 log and 1.97 log CFU/ml, respectively). Counts of psychrotrophs were significantly higher for immersion chilled carcasses than air-chill carcasses (3.20 log and 1.91 log CFU/ml, respectively). The incidence of Salmonella spp. and Campylobacter spp. were reported lower in air-chilled broilers due to a higher prevalence of crosscontamination among immersion-chilled broilers.

Huffman (2002) noted that hot water applications also have potential of reducing bacterial counts on beef carcasses by 1–3 log cycles. Barkate et al. (1993) reported that when the surface temperature of beef carcasses was raised to 82 °C for about 10 s using hot water sprays (95 °C), a significant reduction in bacterial numbers was observed between control and hot water-treated carcass surfaces. Castillo et al. (1998b) likewise reported that a water wash followed by hot water spray (95 °C) reduced levels of for Escherichia coli O157:H7, S. Typhimurium, APC, and coliforms by 3.7, 3.8, 2.9, and 3.3 log, respectively, on carcass surfaces. Spray-washing (26 °C, 276 kPa followed by 1,000 kPa) followed by hot-water rinsing (>77 °C, 138–152 kPa, 2.5–8 s) and knife-trimming followed by a second spray-wash also have been shown to be an effective beef carcass decontamination method (Delmore et al. 1997). Gorman et al. (1995) concluded that hot water (74 °C at the surface of the sample) applied as a spray washing process onto the beef surfaces caused reductions in bacterial counts exceeding 3.0 log CFU/cm2 when compared to the combination of hand-trimming and spray-washing with colder (<35 °C) water. In summary, hot water treatment (>74 °C) of beef carcasses is a common practice in the industry and the data indicate that hot water applications to carcasses have been effective to reduce bacterial counts by 1–3 log cycles. However, water temperature, water pressure, carcass coverage, and dwell time are needed to take into consideration to effectively implement and validate hot water as a decontamination step (Huffman 2002).

Application of steam to accomplish thermal destruction of bacteria on the surface of meat carcasses has been considered as an alternative to hot water spraying. A commercial antimicrobial carcass intervention process called steam pasteurization which was approved by the FDA in 1995 for whole carcasses as well as parts of carcasses that are to be further processed has been adopted by the industry (Chen et al. 2012). Nutsch et al. (1997) evaluated effectiveness of a steam pasteurization process for reducing naturally occurring bacterial populations on freshly slaughtered beef sides in a large commercial facility. The results indicated that steam pasteurization is very effective in a commercial setting for reducing overall bacterial populations on freshly slaughtered beef carcasses. Steam pasteurization process includes exposing meat carcasses and meat products to water steam at 82–97 °C inside a chamber or a tunnel at atmospheric pressure for 6–12 s. The treatment consists of three steps; water removal, steam pasteurization, and rapid chilling (Aymerich et al. 2008; Chen et al. 2012). Phebus et al. (1997) reported that the steam pasteurization consistently produced numerically greater pathogen reductions than knife-trimming or hot water/steam vacuum spot cleaning on beef carcasses and the reductions for all three treatments ranged from 2.5 to 3.7 log CFU/cm2. All three treatments were also more effective than water washing (35 °C) which gave only a reduction of 1.0 log CFU/cm2. Likewise, Nutsch et al. (1998) evaluated a steam pasteurization system in a commercial beef processing facility and found significant reductions in total aerobic plate counts and E. coli counts at five separate anatomical locations on the carcasses. Avens et al. (2002) reported application of flowing steam at 98 °C for 3 min virtually destroyed aerobic bacteria on the skin of naturally contaminated poultry carcasses. In another study, Whyte et al. (2003) exposed the broiler carcasses to atmospheric steam at 90 °C for 24 s which was provided reductions of 0.75, 0.69, and 1.3 log CFU/g in total viable counts, Enterobacteriaceae, and Campylobacter counts, respectively. However, they also reported visible damages to the outer epidermal skin tissue of carcasses following the steam pasteurization.

A variation of the steam pasteurization called steam vacuuming has been developed and adopted by the industry to remove fecal and visible contamination which is less than 2.54 cm at its greatest dimension on carcasses. Steam vacuum systems consist of two sequential steps including steam or hot water spray (82–88 °C) on a small, designated carcass area and then vacuuming using a handheld device developed for this purpose. Thus, combined effect of removing and inactivating surface contamination can be achieved on the carcasses (Huffman 2002). Dorsa et al. (1997) examined application of steam vacuum and hot water washes on beef carcass surfaces. They concluded that the use of steam vacuum and hot water effectively reduces bacterial populations from beef carcass tissues immediately after treatment with reductions of up to 2.7 log CFU/cm2 for APC, lactic acid bacteria, and L. innocua and as much as 3.4 log CFU/cm2 for E. coli O157:H7. Castillo et al. (1999a) indicated that steam vacuuming reduced the number of different indicator organisms around 3.0 log cycles but also spread the bacterial contamination to areas of the carcass surface adjacent to the contaminated sites. However, they suggested that a combined treatment including steam vacuuming followed by spraying with hot water and then lactic acid effectively reduced the relocated contamination.

2.2 Carcass Trimming

Although trimming has been considered for completely removing the physical contamination including fecal and other visible contaminants and pathogens, under the commercial slaughtering conditions, trimming has been reported to be a highly variable process since the efficacy of the trimming primarily related to the skill and carefulness of the individual who is applying the trimming. In addition, spreading the contamination due to improperly sanitized equipment used during trimming and holding the carcasses for trimming at the warm slaughter room temperature raise questions about the actual efficacy of trimming as a method of reducing pathogen contamination of carcasses (Reagan et al. 1996; Castillo et al. 1998a; Edwards and Fung 2006). In a comparative study, Reagan et al. (1996) examined treatment procedures included trimming, washing, and trimming followed by washing under the industrial conditions. Their results indicated trimming followed by washing produced approximately 2 log CFU/cm2 reduction in aerobic bacteria, while trimming alone which was done by industry personnel at normal slaughtering speeds and operating practices, reduced contamination by approximately 1.3 log CFU/cm2. The mechanism of removing visible contamination by use of the trimming followed by washing was explained as a combination of physical removal by trimming with additional removal of debris and foreign material by washing. They also indicated that some visible contaminates were left on the carcasses following the trimming alone due to the possible accidental recontamination. Similarly, Delmore et al. (1997) reported that decontamination of beef carcasses could be achieved by knife trimming followed by spray washing or by spray washing followed by hot water rinsing. Likewise, water wash or trimming as a single beef carcass intervention was reported not sufficient for significantly reducing pathogens on beef carcasses (Castillo et al. 1998a). Laster et al. (2012) reported that trimming of external fat surfaces during the normal fabrication process may reduce contamination of E. coli O157:H7. However, fat and lean surfaces that were not inoculated became contaminated during the fabrication process. They concluded that trimming external surfaces reduced levels of pathogens, but under normal fabrication processes, pathogens were still spread to newly exposed surfaces.

2.3 Irradiation

Ionizing radiation has been described as radiation that has enough energy for removing electrons from atoms, thus leading to the formation of ions. While there are different types of ionizing radiation, gamma-rays produced from the radioisotopes Cobalt 60 (1.17 and 1.33 MeV) and Cesium 137 (0.662 MeV), X-rays generated from a machine operated at or below 5 MeV, and machine-generated electron beams (maximum energy 10 MeV) are permitted for food irradiation to inactivate microorganisms including pathogens (Dincer and Baysal 2004; Pillai 2004; Chen et al. 2012). Cobalt 60 is used by the majority of facilities in the industry due to stronger gamma ray producing ability and lack of water solubility. Alternatively, electron beams produced by commercial electron accelerators have the advantage of switching the system on and off like any other electrical apparatus and they can be used for removing surface contamination of meat and poultry products. Lastly, producing X-rays requires slamming fast moving electrons into a metal objects. Strong X-ray that has an energy superior to 1 MeV can be produced using tantalum or platinum targets with the possibility of processing packaged meat products in large quantities (Aymerich et al. 2008).

Regardless of the source and the facility generating irradiation, the main target of the irradiation is the molecular bonds in the microbial DNA. In addition to damages to DNA, denaturation of enzymes and cell membrane alteration may also occur with the irradiation. RNA is likewise a target for ionizing radiations since lethal effects of irradiation on RNA containing viruses have been observed. Nucleic acids can also be damaged by an ionized adjacent molecule such as water that produces a lethal product for the genetic material. Water molecules lose an electron due to ionizing radiation and produce H2O+ and e−. A number of compounds including hydrogen, hydroxyl radicals, molecular hydrogen, oxygen, and hydrogen peroxide are then produced with the reactions of water molecules. The most reactive of them are the hydroxyl radicals (OH•) and hydrogen peroxide (H2O2). All of these byproducts react with other water molecules, nucleic acids, and other biologically sensitive molecules. Although biological systems have a repair capacity of both single- and double-stranded breaks of the DNA backbone, ionizing radiation at doses used in food irradiation is probably causing damages so extensive that bacterial repair of the damages become nearly impossible (Pillai 2004; Aymerich et al. 2008).

Application of ionizing radiation to frozen and chilled poultry with doses of 3–5 and 1.5–2.5 kGy, respectively, reduced Salmonella by about 3 log units (Corry et al. 1995; Farkas 1998; Buncic and Sofos 2012). Similarly, aerobic bacteria were reduced around 3.0 log CFU/g on chicken legs by irradiation of 1 kGy (Loretz et al. 2010). Sarjeant et al. (2005) stated that electronic beam irradiation reduced inoculated S. Typhimurium on fresh chicken breasts about 4 log units with doses of 1, 2, or 3 kGy. Likewise, gamma radiation was reported effective for inactivating psychrophiles and Enterococcus bacteria on turkey breast samples which were irradiated at doses from 1 to 3 kGy (Henry et al. 2010). Exposure of poultry viscera to a higher dose of gamma radiation (20 kGy) rendered the viscera sterile, while 5 and 10 kGy decreased the total bacterial count by 4 and 6 log cycles, respectively, and eliminated the coliforms to <1 CFU/g of tissue (Jamdar and Harikumar 2008). Arthur et al. (2005) reported that low-dose, low-penetration electron beam irradiation (dose of approximately 1 kGy with a depth penetration of 15 mm) reduced E. coli O157:H7 on beef carcass surfaces by at least 4 log CFU/cm2 indicating potential use of the treatment as an antimicrobial intervention on beef carcasses during processing.

2.4 High Pressure Processing Systems

High pressure processing (HPP) also called hydrostatic pressure (HHP) or ultrahigh pressure processing (UHP) is primarily applied as a batch process to prepackaged food products using a chamber surrounded by water or another pressure-transmitting fluid. The food products usually are vacuum-packaged in a flexible package and placed in the pressure vessel and then submitted to pressures ranging from 100 to 900 MPa. However, the pressure levels of 400–600 MPa are mostly used in commercial applications depending on the product for 3–5 min. Following the pressure treatment, the processed product is removed from the vessel and stored or distributed in a conventional manner. Several factors have been reported to contribute to the inactivation of microorganisms by HPP including changes in the cell membranes, cell wall, proteins, and enzyme-mediated cellular functions. The primary sites damaged by the pressure are cell membranes with subsequent alterations of cell permeability, transport systems, loss of osmotic responsiveness, organelle disruption, and inability to maintain intracellular pH (Simpson and Gilmour 1997a, b; Campus 2010).

HPP application of 700 MPa at 15 °C for 1 min was reported causing up to 5 log reduction of E.coli O157:H7 in raw minced meat and increasing the shelf-life of the raw minced meat under refrigerated conditions (Gola et al. 2000). Similarly, Morales et al. (2008) found that multiple-cycle treatments of HPP resulted with a higher E. coli O157:H7 lethality than single-cycle treatments since the single-cycle treatments at 400 MPa and 12°C ranged from 0.82 log CFU/g for a 1 min cycle to 4.39 log CFU/g for a 20 min cycle while multiple-cycle treatments produced reduction of 4.38 log CFU/g with four 1 min cycles at 400 MPa and 12°C and 4.96 log CFU/g with three 5-min cycles. Garriga et al. (2004) reported that the safety risks associated with Salmonella and L. monocytogenes in sliced marinated beef loin stored up to 120 days at 4 °C was reduced with HPP treatment at 600 MPa and 31 °C for 6 min.

3 Chemical Decontamination Treatments

Consumers, especially in developed countries, demand high quality and safe meats nowadays. To meet the consumer demand and as a response to the USDA-FSIS mandate to increase the safety of meat and poultry products, numerous chemical compounds have been evaluated as decontamination agents. The chemical interventions include various food-grade chemicals that are usually applied to the meat surface, to inhibit or kill microorganisms. The mode of action of the chemicals is mainly due to their ability to disrupt cellular membranes or other cellular constituents and interrupt physiological processes (Loretz et al. 2010). Chemical compounds must be proven effective and approved for use by the U.S. Food and Drug Administration (FDA) and the USDA-FSIS before used as a decontamination agent. Once proven to be safe, antimicrobials may be applied to carcass or product surfaces. These compounds that are naturally derived or manufactured should not conceal spoilage, but should extend shelf life and prevent pathogen growth as a consequence of their bactericidal or bacteriostatic activity (Keeton and Eddy 2004). This section will focus on chemical decontamination treatments currently available to the meat industry, such as organic acids, chlorine-based treatments, trisodium phosphate, electrolyzed water, acidic calcium sulfate, epsilon polylysine, and lauric arginate.

3.1 Organic Acids

Solutions of organic acids (1–3 %), such as lactic and acetic acids, are commonly used for beef and lamb (Chen et al. 2012). An organic acid spray is the most commonly used means of chemical decontamination of beef carcasses in combination with steam vacuuming, hot water washing, or steam cabinets (Huffman 2002). Bolton et al. (2001) reported that organic acids such as lactic or acetic acid are usually applied using a spray cabinet and recommended critical limits including at least 500 mL of a 2.5–10 % (v/v) acid (to allow for dilution when applied to the carcass) maintained at a pH of ≤ 2.8 and temperature of 25°–55 °C and sprayed for 35 s at 13.8–27.6 Pa for an organic acid spray application. Even though the mechanism for the antimicrobial activity of organic acids is not completely known, it is generally believed that the undissociated form of the acid, or its ester, is responsible for the activity. Weak acids penetrate the bacterial cell membrane and accumulate in the cytoplasm, and the protonated acid acidifies the cytoplasm if the intracellular pH is higher than the pKa of the acid, resulting in cell injury or death (Keeton and Eddy 2004).

Hardin et al. (1995) found that beef carcass washing followed by warm acid sprays (55 °C) of lactic acid or acetic acid performed better than trimming or washing alone for reducing Salmonella and E. coli O157:H7 and that lactic acid was more effective than acetic acid for E. coli O157:H7 reduction. In another study, both a water wash and trimming combined with sanitizing treatments of hot water (95 °C) or warm (55 °C) 2 % lactic acid spray or a combination of these two sanitizing methods resulted in reductions of more than 4.0 log CFU/cm2 for S. Typhimurium and E. coli O157:H7 on beef carcasses (Castillo et al. 1998a). Further, Castillo et al. (2001b) found that prechill treatment of 2 % lactic acid spray (250 ml, 55 °C) reduced the counts of S. Typhimurium and E. coli O157:H7 on beef carcass surfaces that had been inoculated. In addition, a 4 % l-lactic acid spray at 55 °C prior to fabrication has also been suggested for chilled beef carcasses which were previously subjected to a hot water spray followed by a lactic acid spray prior to chilling (Castillo et al. 2001a). In a comparative study, King et al. (2005) reported that a peroxyacetic acid spray was not an effective intervention for S. Typhimurium and E. coli O157:H7 reduction on chilled beef carcasses when compared to carcasses treated with 2 % l-lactic acid spray before chilling or 4 % l-lactic acid spray after chilling. Similarly, Dorsa et al. (1998a) suggested that a 2 % lactic acid or 2 % acetic acid wash during beef carcass processing could lower the bacterial counts in ground beef.

Sakhare et al. (1999) found that acetic acid (0.5 %) or lactic acid (0.25 %) treatments applied by either dipping or spraying after scalding, defeathering, and evisceration of chicken carcasses were more effective than spray washing with water alone to decrease crosscontamination and improve microbial quality. In a comparative study Sinhamahapatra et al. (2004) reported that lactic acid dip and hot water dip were the most effective for reducing aerobic plate counts by 1.36 log and 1.28 log/cm2 on broiler carcasses. Treatments with acetic acid or lactic acid by either dipping or spraying after scalding, evisceration, and defeathering have been claimed to decrease crosscontamination and improve the microbial quality of chicken carcasses (Sakhare et al. 1999). Yoder et al. (2012) studied eight antimicrobial compounds (acetic acid, citric acid, lactic acid, peroxyacetic acid, acidified sodium chlorite (ASC), chlorine dioxide, sodium hypochlorite, and aqueous ozone) applied at various concentrations with small, handheld spraying equipment for suitable to use in very small meat plants. Relative antimicrobial effectiveness of the compounds was determined as organic acids > peroxyacetic acid > chlorinated compounds > aqueous ozone. A comparative study of acetic, citric, lactic, malic, mandelic, propionic, and tartaric acids against S. Typhimurium attached to broiler skin found that concentrations of greater than or equal to 4 % of the acids were required to kill greater than or equal to 2 log number of the pathogen (Tamblyn and Conner 1997).

3.2 Chlorine-Based Treatment

Chlorinated water is used to control microbial contamination and growth in the meat industry. The chlorine levels do not normally exceed 50 ppm, which results in a reduction in microbial load of 1 log cycle (Bolder 1997). However, Northcutt et al. (2005) conducted a study to investigate the microbiological impact of spray washing broiler carcasses with chlorinated water (0 or 50 ppm) at different temperatures (21.1, 43.3, or 54.4 °C). They concluded neither adding chlorine nor elevating the water temperature during spray washing in an inside–outside bird washer did enhance the removal of bacteria from broiler carcasses. Similarly, Keeton and Eddy (2004) indicated that use of chlorinated water (20–50 ppm) to reduce the pathogen load on poultry carcasses at the prechill washer or in the chill tank have had mixed results and chlorinated water is less effective than other compounds such as hypochlorite, chlorine dioxide, ASC, and cetylpyridinium chloride (CPC).

Efficacy of 200 ppm hypochlorite on the bacterial counts has been reported on beef carcasses with some residual effect during refrigerated storage. However, its use as a carcass decontamination agent is limited due to effectiveness of other chemicals (e.g., organic acids) against pathogens which is generally more than hypochlorite (Keeton and Eddy 2004). In contrast, chilling poultry carcasses with 20 ppm sodium hypochlorite solution reduced coliforms, Campylocater, E. coli, and Salmonella counts by 1.2, 1.3, 1.4, and 0.5 logs, respectively (Northcutt et al. 2003a).

Disinfecting public water supplies using chlorine dioxide is a common practice in the industry. Chlorine dioxide is also promising as a decontamination agent for carcass surfaces. The mode of action of chlorine dioxide is due to the irreversible damage to fatty acids and proteins in the bacterial cell membrane, resulting in the loss of permeability and the destruction of the transmembrane ionic gradient (Keeton and Eddy 2004). Beef trimmings were treated with 200 ppm chlorine dioxide to reduce inoculated E. coli and S. Typhimurium but only 0.71 and 0.61 log CFU/g declines were observed, respectively, in ground beef manufactured from trimmings (Stivarius et al. 2002). Likewise, Cutter and Dorsa (1995) indicated that spraying beef carcass tissues with chlorine dioxide at a concentration of 20 ppm was not effective for reducing fecal contamination on beef regardless of duration of the spraying. Berrang et al. (2011) reported that application of 50 ppm of chlorine dioxide during defeathering of poultry carcasses produced significantly lower numbers of Campylobacter and E. coli and a lower prevalence of Salmonella than carcasses treated with the water spray as control defeathering.

ASC is an acid-activated, broad spectrum antimicrobial approved by the USDA-FSIS as an antimicrobial agent for use on poultry and beef (Keeton and Eddy 2004; U.S. Department of Agriculture Food Safety and Inspection Service 2013). As a processing aid ASC does not require labeling with insignificant residue levels. In poultry operations, ASC is mostly applied at the end of the evisceration line before or after carcass chilling. Similarly ASC is generally applied as a carcass rinse after evisceration or to trimmings immediately before grinding in red meat operations. Effectiveness of ASC has been shown against pathogens (E. coli O157:H7, Listeria, Campylobacter, Salmonella), viruses, fungi, yeast, molds, and some protozoa. Acidification of NaClO2 forms HClO2(ASC) and then ASC and organic matters react to form several oxychlorous intermediates which are broad-spectrum germicides. Then these compounds break oxidative bonds (sulfide and disulfide linkages) on the bacterial cell membrane surface and kill the cell. The reaction residues are primarily chloride and chlorate salts (Keeton and Eddy 2004). ASC must be used in combination with any GRAS acid at a level sufficient to achieve a pH of 2.3 or 2.9 depending on the meat or poultry product (U.S. Department of Agriculture Food Safety and Inspection Service 2013). In a comparative study, Sinhamahapatra et al. (2004) tested the effects of hot water (70 °C for 1 min), 2 % lactic acid (30 s), 1,200 ppm ASC (5 s), and 50 ppm chlorine solution (5 min) applied to broiler carcasses as an immersion or spray treatment. The lactic acid dip and hot water dip were the most effective for reducing aerobic plate counts by 1.36 log and 1.28 log/cm2, respectively, whereas ASC and a hot water dip reduced presumptive coliforms counts by 1.37 log and 1.34 log/cm2. Similarly, Del Rio et al. (2007) reported that 1,200 ppm ASC immersion solutions were effective on chicken legs for reducing microbial population including mesophilic aerobic counts, psychrotrophs, Enterobacteriaceae, coliforms, Micrococcaceae, enterococci, Brochothrix thermosphacta, pseudomonads, lactic acid bacteria, molds, and yeasts during 5 days of storage at 3 °C. Kemp et al. (2000) indicated that ASC treatment was an effective method for significantly reducing naturally occurring microbial contamination on carcasses and the highest antimicrobial activity was achieved with prewashing and then exposing to a 5 s dip in a solution containing phosphoric acid- or citric acid-activated ASC. Their results showed that a 5 s dip in 500–1,200 ppm ASC reduced total aerobes by 82.9–90.7 %, E. coli by 99.4–99.6 %, and total coliforms by 86.1–98.5 % on poultry carcasses before chilling. In another study, both E. coli O157:H7 and S. Typhimurium counts on beef carcasses were reduced by 3.8–3.9 log and 4.5–4.6 log with a water wash followed by a phosphoric acid-activated acidified sodium chloride spray or a citric acid-activated ASC spray, respectively (Castillo et al. 1999b).

CPC is a quaternary ammonium compound which is a water-soluble, colorless, and neutral pH. Levels of 0.05–0.5 % CPC are used to reduce or inhibit gingivitis and biofilm and plaque formation in mouthwashes (Cutter et al. 2000; Keeton and Eddy 2004). CPC penetrates and destroys bacterial cell walls and cell membrane and kills bacteria by the interaction of basic cetylpyridinium ions reacting with the acid groups of bacteria to form weakly ionized compounds that inhibit bacterial metabolism (Li et al. 1996; Keeton and Eddy 2004). In a model system, 4.87 logs CFU/cm2 of S. Typhimurium reduction was observed following 0.4 % of CPC application to chicken skin for 3 min (Breen et al. 1997). Li et al. (1996) found that spraying contaminated poultry skin with 0.1 % CPC reduced Salmonella by 0.9–1.7 logs CFU/cm2, similar reductions were also obtained (1.0–1.6 logs CFU/cm2) when the poultry skin was immersed in CPC. Cutter et al. (2000) determined the effectiveness of 1 % CPC spray (862 kPa, 15-s, 35 °C) against pathogens associated with lean and adipose beef surface. S. Typhimurium and E. coli O157:H7 were immediately reduced by a 1 % CPC solution on lean beef from 5 to 6 logs CFU/cm2 to undetectable levels while pathogen counts were reduced to <2.5 logs CFU/cm2 on fat tissues. The pathogen counts on lean tissue were undetectable following 35 days of storage at 4 °C but counts on fat tissue remained at <1.3 log CFU/cm2. Even though CPC was proven to effectively reduce pathogenic bacteria on beef tissues residual CPC levels following any of the treatments exceeded those for human consumption.

3.3 Trisodium Phosphate

As a very alkaline (pH 12–13) antimicrobial ingredient, trisodium phosphate (TSP) has been approved for use as a spray or dip for on raw poultry carcasses and giblets (U.S. Department of Agriculture Food Safety and Inspection Service 2013). TSP is applied to poultry carcasses or parts up to 15 s using an 8–12 % solution within a temperature range of 18.3°–29.4 °C. Similarly, the giblets are sprayed or dipped for a minimum of 30 s with an 8–12 % solution. TSP’s antimicrobial effect is apparently the result of disruption of cytoplasmic cell membrane followed by the leakage of internal contents and phase separation of the cytoplasm into dark and light zones due to water solubility of the bacterial DNA at high pH (Mendonca et al. 1994; Keeton and Eddy 2004).

Kim et al. (1994) reported that trisodium phosphate reduced Salmonella by 1.6–1.8 logs when post-chill poultry carcasses were dipped into a 10 % solution at 50 °C for 15 s. In a different study, experiments were conducted to determine the effect of TSP treatment on reducing salmonellae recovery from broiler carcasses immediately after chilling or following 7 days of storage. Carcasses were subjected to a 5-s dip in 10 % TSP solution. The results indicated that a prechill trisodium phosphate treatment reduced salmonellae-positive samples immediately after chilling or following 7 days of storage on broiler carcasses (Bourassa et al. 2004). In a comparative study, Li et al. (1997) tested 0.85 % sodium chloride, 5 or 10 % trisodium phosphate, 5 or 10 % sodium bisulfate, 0.1 % CPC, or 1 % lactic acid sprays on prechilled chicken carcasses. They reported that spraying 10 % trisodium phosphate for 90 s reduced S. Typhimurium by 3.7 logs while 2.4, 1.6, and 1.6 logs of reductions were obtained for 10 % sodium bisulfate, 0.1 % cetylpyridinium, and 1 % lactic acid, respectively.

Potential use of TSP solutions as a decontamination treatment has investigated in a few studies for beef carcasses. Kim and Slavik (1994) evaluated TSP for removing attached E. coli O157:H7 and S. Typhimurium from beef surfaces. Fat and fascia surfaces inoculated with E. coli O157:H7 and S. Typhimurium rinsed with a 10 % TSP (10 °C) solution for 15 s. Compared to controls, the levels of E. coli O157:H7 were 1.35 and 0.92 logs lower on TSP treated fat and fascia surfaces, respectively while S. Typhimurium were 0.91 and 0.51 logs lower, respectively. Ramirez et al. (2001) tested a water rinse followed by either a 2 % lactic acid (9 s, at 55 °C) or a 12 % trisodium phosphate (60 s, at 55 °C) dip or a combination of these treatments. Both treatments alone or in combination were effective for reducing E. coli O157:H7 by more than 1.6 log/cm2 on lamb breast tissue. In contrast, Dorsa et al. (1998b) tested the effect of 2 % lactic acid, 2 % acetic acid, 12 % TSP, and water washes at 72 and 32 °C for reducing pathogens and other bacterial populations on beef carcass surfaces and cuts held for up to 21 days (4 °C) under vacuum. They reported that TSP was not as effective as organic acid treatments for growth suspension on beef surfaces and in some cases the effect was similar to untreated samples. Conversely, 10 % trisodium phosphate or 0.5 % CPC treatment applied by tumbling significantly reduced E. coli O157:H7 and S. Typhimurium and improved the redness of ground beef (Pohlman et al. 2002).

3.4 Other Chemical Treatments

Antimicrobial activity of some other chemicals including electrolyzed water, acidic calcium sulfate, ε-polylysine, and lauric arginate were also evaluated for the decontamination of meat and poultry in the literature. Electrolyzed water (EW) is getting popular as a sanitizer in the food industries for reducing bacterial populations on foods and processing surfaces. A dilute sodium chloride solution is dissociated by electrolysis into acidic electrolyzed water (AEW) and basic electrolyzed water (BEW). AEW has a pH of 2–3, an oxidation–reduction potential of >1.100 mV and an active chlorine content of 10–90 ppm, whereas BEW has a pH of 10–13 and an oxidation–reduction potential of −800 to −900 mV. It was reported that AEW reduced vegetative cells of various bacteria in suspension more than 6.0 log CFU/ml. However, reductions were limited for chicken carcasses ranging from about 0.8 to 3.0 orders of magnitude (Hricova et al. 2008; Loretz et al. 2010). Park et al. (2002) evaluated effectiveness of EW for killing Campylobacter jejuni on chicken wings. They found that EW was as effective as chlorinated water in reducing Campylobacter jejuni on poultry meat by about 3 log CFU/g. Similarly, Northcutt et al. (2007) reported that washing poultry carcasses with EW is slightly better (total aerobic bacteria and E. coli) or equivalent to (Campylobacter and Salmonella) washing with sodium hypochlorite in an inside–outside bird washer. In a comparative study, it was demonstrated that EW could reduce S. Typhimurium on poultry surfaces following extended refrigerated storage and could provide poultry establishments with an inexpensive and easy alternative to chlorine treatments to control pathogens during processing (Fabrizio et al. 2002).

A blend of organic acid–calcium sulfate, known as acidic calcium sulfate (ACS), is a very acidic (pH 1.0–1.5) decontamination agent for meat and poultry products that is approved by USDA-FSIS (Keeton and Eddy 2004; U.S. Department of Agriculture Food Safety and Inspection Service 2013). A combination of ACS plus organic acids has been reported to disable the proton pumps in bacterial membranes and thus serve as a metabolic inhibitor (Keeton et al. 2002). The effectiveness of ACS as a surface decontamination agent for reducing pathogens on beef or poultry carcasses or RTE meat products has been reported in several studies (Huffman 2002; Keeton et al. 2002, 2006; Dickens et al. 2004; Nunez de Gonzalez et al. 2004; Zhao et al. 2004; Keeton and Eddy 2004; Luchansky et al. 2005). Another antimicrobial, ε-polylysine (EPL), is a cationic homopolymer of 25–35 l-lysine residues connected at the ε-amino and α-carboxyl group juncture (Geornaras et al. 2007). EPL is an edible, water-soluble agent with a wide range of antimicrobial activity that includes both Gram-positive and Gram-negative bacteria (Yoshida et al. 2002; Yoshida and Nagasawa 2003; Geornaras and Sofos 2005; Geornaras et al. 2007). EPL has been reported to be nontoxic in an acute oral toxicity study in rats with no mortality at concentrations up to 5 g/kg body weight. It was not observed to be mutagenic in bacterial reversion assays and is confirmed safe as a food preservative (Hiraki et al. 2003). Lauramide arginine ethyl ester (LAE), also known as lauric arginate, is an antimicrobial compound derived from lauric acid and arginine with a broad spectrum of antimicrobial activity (Rodriguez et al. 2004; Bakal and Diaz 2005). LAE has been verified to be nontoxic and is metabolized rapidly to naturally occurring amino acids, largely arginine and ornithine after consumption (Ruckman et al. 2004). LAE affects the cyptoplasmic membranes of microorganisms by causing a disruption or instability of the plasma membrane lipid bilayer thus further altering the metabolic process and detaining the cellular cycle (Bakal and Diaz 2005). LAE was confirmed as GRAS by the USDA-FSIS and is considered a safe and suitable ingredient when used in the production of meat and poultry products (U.S. Department of Agriculture Food Safety and Inspection Service 2013).

Dickens et al. (2004) found that spraying with ACS solution (1:1 solution of deionized water and ACS; 4 ml/wing) increased the shelf-life of chicken wings from 7 days to 10 days. Geornaras and Sofos (2005) compared antimicrobial activity of EPL with sodium diacetate, sodium lactate, lactic acid, and acetic acid, against different foodborne pathogens including reduced E. coli O157:H7, S. Typhimurium, and L. monocytogenes in a culture broth medium. They concluded that EPL has minimum inhibitory concentrations of 0.02 % for E. coli O157:H7 and L. monocytogenes, and 0.04 % for S. Typhimurium that EPL inhibited growth of these foodborne pathogens at 24 °C. EPL also has been reported to have enhanced antimicrobial activity when combined with glycine, vinegar, ethanol, and thiamine laurylsulfonate (Yoshida and Nagasawa 2003). Rodriguez et al. (2004) exposed S. Typhimurium and Staphylococcus aureus to their minimal inhibitory concentrations of 32 and 8 μg/ml of LAE, respectively. They observed alterations mainly in the outer membrane of S. Typhimurium and in the cytoplasm of S. aureus after exposure to LAE. Further, the proportions of damaged cells after 24 h contact time were reported as 97 and 56.3 % for S. Typhimurium and S. aureus, respectively.

Benli et al. (2011) evaluated the concept of applying more than one antimicrobial to poultry carcasses to obtain greater reductions than one treatment alone due to different modes of action of individual antimicrobials. They reported that sequential spray applications of 300 mg of EPL per liter followed by 30 % ACS and of 200 mg of LAE per liter followed by 30 % ACS produced the highest Salmonella reductions on inoculated chicken carcasses, by 2.1 and 2.2 log CFU/ml, respectively. Similarly, Njongmeta et al. (2011) also reported that sequential application of warm ACS, followed by EPL significantly reduced inoculated levels of S. typhimurium, E. coli O157:H7, and L. monocytogenes with an extended effect over 7 storage days. These studies indicated that using sequential, multi-hurdle interventions might be a better strategy than applying single decontamination treatment to obtain significant reductions in pathogen numbers on poultry and beef carcasses.

4 Conclusion

Safety of meat and poultry products is an important public health concern in most of the countries. Although maintenance of good hygiene practices is an important part of the meat and poultry production, preventing carcasses from pathogen contamination cannot be guaranteed. Application of sequential or multiple-intervention decontamination systems including physical or chemical decontamination treatments or emerging technologies such as hot water washing, steam application, steam vacuuming, carcass trimming, irradiation, HPP, organic acids, chlorinated water, hypochlorite, chlorine dioxide, ASC, CPC, trisodium phosphate, electrolyzed water, acidic calcium sulfate, ε-polylysine, and lauric arginate can greatly reduce or eliminate the pathogens in meat and poultry products.