Uses of Chemical Technologies for Meat Decontamination

In many Asian countries, chlorine continues to be the most widely utilized poultry meat sanitizer (Chousalkar et al., 2019). Comparatively, chlorine has a lower cost than other sanitizers, and ease of use may get inactivated rapidly when comes in contact with meat (Sinhamahapatra and Biswas, 2021). Chlorine is an antimicrobial agent that has been shown to cause membrane permeabilization in both Gram-negative (Yersinia enterocolitica and Escherichia coli) and Gram-positive (Salmonella, Listeria monocytogenes and Bacillus subtilis) bacterial species (Virto et al., 2005).

Chlorine dioxide, hypochlorite, cetylpyridinium chloride (CPC), and acidified sodium chlorite (ASC) could be used as an effective alternative to chlorine (Sinhamahapatra and Biswas, 2021). Also, chlorinated compounds are often combined with organic acids, ozone, and alternative antimicrobials to improve the effectiveness of eliminating pathogens from meat surfaces (Giménez et al., 2024). There is extensive research on the use of various chlorine forms in meat decontamination, making them among the first chemical decontamination methods adopted by the meat industry. Lu et al. (2019) found that chlorine had significant reductions in Campylobacter loads. In a study conducted by Stivarius et al. (2002), minced beef that had been contaminated with E. coli and Salmonella Typhimurium was treated with a solution containing 200 ppm of chlorine dioxide. The results indicated reductions in bacterial counts of 0.44 Log CFU/g for E. coli and 0.82 Log CFU/g for S. Typhimurium. Additionally, Ransom et al. (2003) identified lactic acid and ASC as the highest-potency antimicrobial agents available for use. McWhorter et al. (2023) compared the effectiveness of PAA and ASC in reducing natural microbial contamination on chicken meat, finding both treatments significantly reduce bacterial loads, with potential variations in efficacy depending on specific conditions. Acidifying the sodium chlorite solution with phosphoric acid led to a 3.8–3.9 Log cycle reduction of both pathogens. However, Gill and Badoni (2004) noted that ASC had minimal impact on reducing aerobic bacteria, coliforms, and E. coli on meat.

Trisodium phosphate (TSP) is a highly alkaline antimicrobial agent (pH 12–13) that is authorized for utilization as a spray or immersion on chicken and as a scalding agent. For decontamination, a solution of 8% to 12% TSP could be used on poultry at temperatures between 65°C–85°C for up to 15 s (Alonso-Calleja et al., 2024). Alonso-Calleja et al. (2024) TSP reduced bacterial contamination in the meat and influenced the sensory properties and instrumental color of the meat, with notable effects on both appearance and texture. TSP’s antimicrobial effect is owing to its ability to disrupt cell membranes and enhance the moisture solubility of bacterial DNA at elevated pH levels (Sarjit and Dykes, 2017). TSP has proven effective in eliminating and removing adhered S. Typhimurium from chicken following refrigeration and frozen storage (Yoon and Oscar, 2002). Cutter and Rivera-Betancourt (2000) reported that 10% TSP spray treatments were most effective in lowering S. Typhimurium and E. coli O157 on beef. Using a TSP spray or immersion alone or combined with other pathogen control methods is an effective strategy for lowering pathogenic bacteria in meat. However, challenges in using TSP include problems like handling the highly alkaline treatment solution and the risk of significant corrosion to the device and facilities due to extended contact with the decontaminant.

Research into the chemical decontamination of meat has extensively focused on using organic acids. Although the antimicrobial mechanisms of organic acids are not entirely known, it is commonly thought that the undissociated molecule plays a key role in their antimicrobial activity (Taylor and Doores, 2020). However, Reis et al. (2012) observed that the inhibitory effect of lactic acid on Gram-negative psychrotrophs was mainly attributed to a decline in pH instead of the existence of the undissociated molecule. The variation in antimicrobial activity among different acids suggests that multiple mechanisms of bacterial toxicity may exist (Guo et al., 2022; In et al., 2013). This indicates that the inhibitory mechanisms of organic acids could differ, and the primary antimicrobial mechanism may vary depending on the microorganism (Guo et al., 2022; In et al., 2013).

Organic acids can be found in two basic forms: pure acids and buffered acids. Pure acids include lactic, propionic, acetic, citric, and benzoic acids, while buffered organic acids are the calcium and sodium salts of propionic, acetic, citric, and benzoic acids (Wikipedia, 2005). Among the various organic acids used for meat carcass decontamination, lactic and acetic acids are the most commonly employed. Acetic acid, a monocarboxylic acid known for its strong odor and flavor, is the primary ingredient in vinegar and is mainly used for seasoning. It has a high solubility in water and is frequently present in brined foods. Acetic acid is generally recognized as safe (GRAS) for various general-purpose applications (Álvarez-Ordóñez et al., 2010). Citric acid, a hydroxy tricarboxylic acid that occurs naturally in many plants, is water-soluble, GRAS, and authorized for use in both fresh and processed meats and poultry. Lactic acid (2-hydroxypropanoic acid), a monocarboxylic acid with a pKa 3.79, is generated during anaerobic respiration or fermentation by various bacterial microorganisms, including lactic acid bacteria (Axelsson, 1998). It exists in two isomeric forms (D- and L-). The L isomer is particularly effective at inhibiting pathogens (McWilliam Leitch and Stewart, 2002). Lactic acid is FDA-approved for use as an antimicrobial agent on meat (both pre-and post-chilling at a 5% acid solution), sub-primal cuts and trimmings (at a concentration of 2%–3% and 55°C), and for washing beef heads and tongues (at concentrations of 2.0%–2.8%).

Most of the studies conducted were on processed meat products and poultry carcasses and a few were on red meat carcasses, and the usage of organic acids on fresh carcasses during slaughter still needs to be further investigated (Aykın-Dinçer et al., 2021; Casas et al., 2021; Han et al., 2020; Omori et al., 2017). Research has indicated that acetic acid is the most effective antimicrobial against S. Typhimurium, with the effectiveness ranking of acetic>lactic>citric>hydrochloric (Álvarez-Ordóñez et al., 2010). Differences in pathogen reductions may be attributed to variables like the temperature of the acid solution, ranging from room temperature to 55°C. The inability to reduce the surface pH of beef that inhibits microbial growth accounted for the lack of reduction in E. coli O157 counts. The efficacy of 4% L-lactic acid for decontaminating chilled carcasses was validated by Gill and Badoni (2004). Minimum inhibitory concentrations of different organic acid salts were assessed in chicken juice for S. Typhimurium, with sodium citrate and sodium lactate showing inhibitory effects at 1.25% concentration at 37°C and 42°C (Milillo and Ricke, 2010). The application of a spray containing a blend of lactic and citric acids to the chicken produced a 1.3 Log CFU/mL reduction of inoculated Salmonella whereas immersing the chicken in the antimicrobial solution for up to 20 s achieved a 2.3 Log CFU/mL reduction (Laury et al., 2009). Citric acid has been found to inhibit S. Typhimurium as effectively as acetic acid (Zhou et al., 2007). Citric acid has proven effective in controlling pathogens in fresh and processed meat. However, the use may be restricted due to potential negative sensory effects and the requirement to maintain a low pH for optimal antimicrobial activity (Zhou et al., 2007). The effectiveness of acetic acid in inhibiting Salmonella contamination can vary significantly based on concentration and specific conditions. Research indicates that acetic acid can effectively reduce microbial load at concentrations as low as 0.25%. This concentration has been shown to completely eliminate Bacillus cereus group, which is known to survive in refrigerated environments (Trček et al., 2015). The utility of the antimicrobial properties of lactic acid has been studied in meat. A 3.4- and 2.8-Log reduction in Salmonella was observed on skins when 10% lactic acid was applied at 55°C (Carlson et al., 2008). Spraying beef trim surfaces with 2.0% and 4.0% lactic acid resulted in 2.0-Log and 1.5-Log reductions of E. coli O157 and Salmonella, respectively (Harris et al., 2006). Özdemir et al. (2006) noted a 1.2 Log CFU/g reduction of S. Typhimurium in beef after a 15-s immersion in hot water (82°C) combined with 2% lactic acid. Lactic acid decreased S. Typhimurium counts by about 2.5 Log CFU/g from the initial inoculation by the 6th day of storage at 4°C, with only slight reductions noted on days 9 and 12 in vacuum-packed chicken (Over et al., 2009). In fresh sausages, deboned chicken meat treated with a 1% lactic acid solution showed a notable decontaminating effect on Salmonella spp. (Deumier, 2006). However, previous reports indicate minimal effectiveness of lactic acid treatment on chilled carcass surfaces, suggesting that further studies are needed to validate its use on meat.

Bacteriocins are small, thermally stable peptides with antimicrobial properties, primarily produced by bacteria such as Lactococcus lactis, Lactobacillus curvatus, and various Streptococcus species (Woraprayote et al., 2016). Proteases break down these peptides and have a minimal impact on the intestinal microbiota (Woraprayote et al., 2016; Zendo, 2013). The study by Casaburi et al. (2016) demonstrates that L. curvatus 54M16 is an effective starter culture for fermented sausage, producing bacteriocins that inhibit harmful bacteria, while also improving the product’s safety and quality. Biscola et al. (2014) show that bacteriocin-producing L. lactis effectively inhibits the growth of halotolerant bacteria in Brazilian charqui. Rivas et al. (2014) investigated the bacteriocin Sakacin Q produced by L. curvatus ACU-1. It examines the bacteriocin’s functional properties and its effectiveness in inhibiting Listeria on the surface of cooked meat, showcasing its potential as a preservative in meat products.

Nisin, a bacteriocin produced by lactic acid bacteria, is the most widely utilized bacteriocin in meat applications. It is regulated by the Expert Committee of the World Food and Agriculture Organization (Food and Drug Administration [FDA], 2017) and is the only bacteriocin approved by the FDA as GRAS for use in meat (FDA, 2017). Several studies have explored the use of nisin for decontaminating beef. Cutter and Rivera-Betancourt (2000) reported reductions of 1.8–3.5 Log/cm² in bacterial counts on beef inoculated with different Gram-positive bacteria after treatment with a nisin solution (5,000 activity units/mL). In another study, combining nisin with 50 mM ethylenediaminetetraacetic acid (EDTA) led to a reduction in counts of S. Typhimurium and E. coli O157 in buffer solutions (Cutter and Rivera-Betancourt, 2000). When applied to inoculated meat, mixtures of nisin with lactate or EDTA resulted in higher reductions compared to other combinations (Cutter and Rivera-Betancourt, 2000). Additionally, Cutter and Rivera-Betancourt (2000) found that immobilizing nisin in calcium alginate gels enhanced its inhibitory effect on Brochothrix thermosphacta on beef surfaces.

Tu and Mustapha (2002) demonstrated that applying nisin and EDTA to meat fully suppressed B. thermosphacta but had no effect on S. Typhimurium. Similarly, Mustapha et al. (2002) found that the effectiveness of nisin (400 U/mL) combined with 2% lactic acid in reducing E. coli O157 on vacuum-packaged beef was similar to that of lactic acid used by itself. Overall, the effectiveness of nisin and other bacteriocins such as pediocin against Gram-negative microorganisms on meat carcasses appears to be limited, unless combined with other antimicrobials. Additionally, there is limited data on the possibility of resistance occurring in organisms that come into contact with nisin.

Lactoferrin, a glycoprotein that binds iron and is present in mammalian milk and colostrum, exhibits significant antimicrobial activity against various foodborne pathogens (Montone et al., 2023). The FDA has designated lactoferrin as GRAS approved its use at a 2% concentration for meat decontamination (Montone et al., 2023). Activated lactoferrin, a patented form of lactoferrin, has been suggested for use in decontaminating meat (Satyanarayan Naidu, 2002). Activated lactoferrin is reported to disrupt microbial adhesion and colonization, removal of microorganisms from surfaces, inhibition of growth, and neutralization of endotoxins (Satyanarayan Naidu, 2002). In one study, treating beef surfaces with a multi-step spray system that included cold water, hot water, lactic acid, and activated lactoferrin resulted in a 99.9% reduction in E. coli O157, compared to a 72.2% reduction when the activated lactoferrin spray was not used (Satyanarayan Naidu, 2002). However, because activated lactoferrin is derived from milk, it could potentially trigger immunoallergic reactions in individuals sensitive to milk proteins (Satyanarayan Naidu, 2002). Research by Soyer et al. (2020) revealed that when used together, activated lactoferrin and rosemary extract inhibited the growth of various bacteria in vitro, such as E. coli and L. monocytogenes. There is currently limited literature on the challenges associated with activated lactoferrin and how it compares to other approved antimicrobial treatments. Additionally, information on the efficacy of lactoferrin in carcass decontamination and how it stacks up against other chemical treatments is scarce. Therefore, further research is needed to evaluate lactoferrin’s potential for commercial implementation in beef carcass decontamination.

Peracetic acid is an organic peroxide created from a balanced blend of acetic acid, hydrogen peroxide, and water (Kitis, 2004). This compound is highly effective against a broad spectrum of pathogens, including bacteria, viruses, fungi, and spores, even when organic matter is present (Park et al., 2014; Rosario et al., 2019). Previous studies (Kalchayanand et al., 2016; Mohan and Pohlman, 2016) investigated the effectiveness of organic acids and peracetic acid as antimicrobial agents to control pathogenic E. coli on beef. They found that these acids could reduce the presence of the pathogen. Scott et al. (2015) evaluated the antimicrobial efficacy of a sulfuric acid and sodium sulfate blend (SSS), PAA, and CPC in reducing Salmonella contamination on inoculated chicken wings. The results showed that all three treatments effectively reduced Salmonella spp. The effectiveness of SSS and PAA was comparable, indicating their potential for controlling Salmonella on chicken wings. Research indicates that peracetic acid outperforms chlorine and chlorine dioxide in inhibiting spoilage and improving meat safety (Ölmez and Kretzschmar, 2009; Ramos et al., 2013). Its superior efficiency is because of its capacity to permeate cell membranes and break down into hydrogen peroxide and acetic acid within the cytoplasm (Kitis, 2004). The inactivation mechanism of peracetic acid involves the release of active oxygen, which oxidizes sulfhydryl groups and sulfur bonds in proteins and enzymes, ultimately causing cell death (Kitis, 2004; Srey et al., 2013). Furthermore, acetic acid lowers the cell’s internal pH, disrupting essential enzymatic activities for protein, DNA, and RNA synthesis (Srey et al., 2013). The significant ATP consumption needed to restore the cell’s original pH also contributes to microbial inactivation (Theron and Lues, 2007).

Peracetic acid has several advantages as a decontaminant. It works rapidly and is effective against a broad spectrum of microorganisms (Rutala and Weber, 2013). Additionally, it is safe for handlers and environmentally friendly, breaking down into acetic acid and water (Park et al., 2014; Rutala and Weber, 2013). The effectiveness of peracetic acid is influenced by factors such as concentration, duration of exposure, microorganism strain, and the food matrix (Rutala and Weber, 2013).