Campylobacter control strategies at postharvest level

Abstract

Campylobacter is highly associated with poultry and frequently causes foodborne illness worldwide. Thus, effective control measures are necessary to reduce or prevent human infections. In this review, Campylobacter control methods applicable at postharvest level for poultry meat during production, storage, and preparation are discussed. Drying and temperature are discussed as general strategies. Traditional strategies such as steaming, freezing, sanitizing, organic acid treatment, and ultraviolet light treatment are also discussed. Recent advances in nanotechnology using antibacterial nanoparticles and natural antimicrobial agents from plants and food byproducts are also discussed. Although advances have been made and there are various methods for preventing Campylobacter contamination, it is still challenging to prevent Campylobacter contamination in raw poultry meats with current methods. In addition, some studies have shown that large strain-to-strain variation in susceptibility to these methods exists. Therefore, more effective methods or approaches need to be developed to substantially reduce human infections caused by Campylobacter.

Introduction

Campylobacter is a major foodborne pathogen worldwide (Dewey-Mattia et al., 2018; European Food Safety Authority and European Centre for Disease Prevention and Control, 2021; Kirk et al., 2015; Lee and Yoon, 2021). It is a Gram-negative bacterium with a spiral or curved shape and moves via flagella. It is a zoonotic pathogen and highly associated with poultry, which is consistent with the nature of Campylobacter that it can only grow under microaerobic conditions and above 30 °C, with an optimal growth temperature of 42 °C. In addition, an increased concentration of CO₂, generally 5–10% v/v, is required for its growth (Kelly, 2001; Kelly, 2008). Human infection by Campylobacter is mainly caused by C. jejuni and C. coli with C. jejuni being more common than C. coli. It leads to a diarrheal disease with symptoms of fever and abdominal pain (Blaser and Engberg, 2008).

Several epidemiological studies have shown that Campylobacter is one of the main microbiological agents that causes foodborne illness (Dewey-Mattia et al., 2018; European Food Safety Authority and European Centre for Disease Prevention and Control, 2021). Each year, 500 million cases of campylobacteriosis caused by Campylobacter spp. are found worldwide (Chlebicz and Slizewska, 2018). In most cases, C. jejuni has been identified as the prime causative agent (Chlebicz and Slizewska, 2018). The major source of campylobacteriosis in humans is contaminated poultry meat, which accounts for between 60 and 80% of all campylobacteriosis cases. In a study of foodborne outbreaks occurring from 2009 to 2015 in the US, Campylobacter was the fourth most common etiological agent causing outbreaks, behind norovirus, Salmonella, and Shiga toxin-producing Escherichia coli (Dewey-Mattia et al., 2018). In Europe, Campylobacter was the most common zoonotic agent and was responsible for more than 60% of all reported zoonotic cases in 2020 (European Food Safety Authority and European Centre for Disease Prevention and Control, 2021).

Although it seems unlikely that Campylobacter survives long under normal atmospheric environmental conditions, its survival is still long enough for it to survive on the surface of food materials, especially chickens, and to infect humans upon consumption. Therefore, effective control strategies against Campylobacter are important for preventing or reducing Campylobacter contamination of food materials and cross-contamination of food contact surfaces. In this review, Campylobacter control strategies at postharvest level, including during production, storage, and preparation, are discussed.

Campylobacter in poultry

As mentioned earlier, Campylobacter is highly adapted to poultry, and many broiler chickens on farms are frequently colonized by Campylobacter, although other animals, such as swine or cattle, are also colonized (Plishka et al., 2021; Sahin et al., 2015). The chickens are usually not colonized until 2 weeks of age (Sahin et al., 2015). Most flocks are colonized at 2 to 3 weeks of age after they are placed in a broiler house (Newell and Fearnley, 2003). In one study, organic and free-range chicken flocks were colonized by Campylobacter at the ages of 14 and 32 days, respectively (Allen et al., 2011).

Contamination of meat usually occurs during processing at the slaughterhouse. The consumption of undercooked poultry meat is a main cause of human campylobacteriosis (Jacobs-Reitsma et al., 2008; Luber, 2009; Myintzaw et al., 2023; Skarp et al., 2016). In addition, the cross-contamination of other food products during the handling of raw poultry meat can contribute to human Campylobacter infection (Luber, 2009; Santos-Ferreira et al., 2021). Many studies have shown that Campylobacter is highly prevalent in poultry meat (Hamad et al., 2023; Szosland-Fałtyn et al., 2018; Tedersoo et al., 2022; Wei et al., 2016; Zhu et al., 2017). For example, 2%, 37%, and 67% of chicken meat samples from Estonia, Latvia, and Lithuania, respectively, were positive for Campylobacter (Tedersoo et al., 2022). In the United States, Campylobacter was found in 4.2% of raw chicken breasts sold at retail (Mujahid et al., 2023). In Egypt, Campylobacter was found in 80% of chicken breasts and 88% of chicken thighs (Hamad et al., 2023). In Poland, Campylobacter was also common in poultry meat, with frequencies of 70%, 38%, 80%, and 60% in chicken, turkey, duck, and goose meat, respectively (Szosland-Fałtyn et al., 2018). In China, 45.1% of chicken carcasses in retail markets were contaminated by Campylobacter among 1587 tested samples (Zhu et al., 2017). In South Korea, 58.8 and 96.2% of chicken and duck meat samples from retail stores, respectively, were contaminated by Campylobacter (Wei et al., 2016).

General control strategies

Campylobacter contamination can be effectively combatted by targeting the inherent attributes of Campylobacter. C. jejuni is known to be susceptible to dry conditions, and maintaining dry conditions is a good strategy for preventing or eliminating Campylobacter contamination in a cost-effective manner (Table 1) (Cox et al., 2001; Doyle and Roman, 1982; Humphrey et al., 1995). As an example, C. jejuni was poorly recovered after 30–60 min of incubation from inoculated dry surfaces of hatchery environments such as chick pads, pine shavings, and eggshell, with water activity of 0.52, 0.61, and 0.98, respectively (Cox et al., 2001). In another study, blood drops containing Campylobacter were placed on laminate surfaces, and one set of drops remained wet by placing in covered petri dishes and another set of drops were dried by exposure to air, occurring within 2 h (Humphrey et al., 1995). After 4 h at 20 °C, Campylobacter survived well in wet drops but did not survive in air-dried drops (Humphrey et al., 1995).

Table 1.

Pros and cons of each method for Campylobacter control

Method	Conditions	Pros	Cons (limitations)	References
Dry conditions	Inanimate surfaces, facilities	Inexpensive	Unsuitable for high-moisture foods	NA
Room temperature	Food contact surfaces; facilities	Inexpensive	Unsuitable for storage of poultry meat	NA
Steam	Foods; food contact surfaces	Rapid heating of surfaces; no wastes; reduced water consumption compared to washing	Bacterial penetration into carcasses by steam pressure; Impairs meat quality; not applicable for heat sensitive surfaces	Castell-Perez and Moreira (2004), James et al. (2007), Sharma et al. (2022)
Freezing	Foods	Acceptable meat quality with no chemical residues	High energy consumption	NA
Sanitizers	Foods; inanimate surfaces; food contact surfaces	No equipment needed	Chemical residues; negative consumer perception; wastes	Hygreeva et al. (2014), Sharma et al. (2022)
Organic acids	Foods	Cheap, simple, and safe	The antimicrobial effect is affected by food pH	Mani-López et al. (2012), Rossi et al. (2023)
Natural antimicrobials	Foods; food contact surfaces; food packaging	Positive consumer perception; environmentally friendly	Less knowledge on the adverse effects	Hygreeva et al. (2014), Sharma et al. (2022)
Nanotechnologies	Foods; food contact surfaces; food packaging	High chemical and physical stability; wide applicability	Lack of research on biosafety; concerns about environmental release	He and Hwang, (2016), Rahmati et al. (2020)
UV	Foods; food contact surfaces	Ease of handling; inexpensive; wide disinfection ranges; environmentally friendly	Low efficiency in opaque or cloudy liquids and solid foods; harmfulness of prolonged exposure	Delorme et al. (2020), Kim and Song, (2023), Ramos et al. (2024)

NA not available

Temperature also affects the survival of Campylobacter. C. jejuni is known to be more susceptible to room temperature than to refrigeration temperatures, and temperature control can be a useful strategy for effectively reducing Campylobacter contamination (Doyle and Roman, 1982; Solow et al., 2003). In the study by Doyle and Roman (1982), the inactivation rate of C. jejuni under dry conditions was much faster at 25 °C than at 4 °C. In another study, C. jejuni and C. coli inoculated on the skins of raw chicken or pork were reduced by 1 to 2 log CFU/cm² after 48 h at 25 °C, while they were not reduced at 4 °C under both aerobic and microaerobic conditions (Solow et al., 2003). When chicken samples inoculated with C. jejuni or C. coli were incubated under aerobic conditions at different temperatures, − 20 °C, 4 °C, and 12 °C, survival was greatest at 4 °C and lowest at 12 °C (Oyarzabal et al., 2010).

Control strategies during production and storage

Steam

Many studies have demonstrated that steam treatment can effectively reduce Campylobacter contamination on chicken carcasses, meat or chicken contact surfaces (Table 2) (Berrang et al., 2020; Boysen and Rosenquist, 2009; Chaine et al., 2013; Cil et al., 2019; James et al., 2007; Kure et al., 2020; Whyte et al., 2003). In one study, Campylobacter contamination was significantly reduced by approximately 2 log CFU per floor square in a broiler transport container after 15 s of steam heating at 100°C (P < 0.05), while no significant reduction occurred after 15 s of water rinsing (Berrang et al., 2020). However, the combined treatment involving a water rinse followed by steam heat was significantly more effective than treatment involving steam heat only (P < 0.05), resulting in a greater than 4 log CFU reduction per floor square. When broiler carcasses were exposed to steam at 90 °C for 24 s, the Campylobacter contamination level decreased by 1.3 log CFU/g (Whyte et al., 2003). Similarly, steam treatment at 95 °C or 120 °C for 3 or 5 s reduced Campylobacter contamination levels in the breasts, legs, thighs, and wings of chicken carcasses by 0.8–4.3 log CFU (Kure et al., 2020). In this study, 5 s of treatment was much more effective than 3 s of treatment at either temperature, while no significant difference was found between treatment at 95 °C or 120 °C. However, such heat-based decontamination often leads to thermal damage to food (Musavian et al., 2022). In addition, steam pressure can cause the pathogens on the surface to easily penetrate the carcasses, which makes it difficult to decontaminate carcasses (Table 1).

Table 2.

Inactivation effects of steam treatment on Campylobacter in previous studies

Mode of contamination	Subjects	Conditions	Log reduction	References
Natural	Broiler transport cages	100 °C, 15 s, 5.2 bar	2.1	Berrang et al. (2020)
	Chicken carcasses	90 °C, 12 s	0.46	Whyte et al. (2003)
	Chicken carcasses	90 °C, 24 s	1.3	Whyte et al. (2003)
Artificial	Chicken skin	100 °C, 8 s	4.0	Chaine et al. (2013)
	Chicken skin	97 °C, 15 s	> 2.8	Cil et al. (2019)
	Chicken skin	133 °C, 3 s	> 2.8	Cil et al. (2019)
	Chicken carcasses	100 °C, 12 s, 1 bar	2.6	James et al. (2007)
	Chicken carcasses	95–120 °C, 3 s, 4.3 bar	0.84–2.0	Kure et al. (2020)
	Chicken carcasses	95–120 °C, 5 s, 4.3 bar	2.5–4.3	Kure et al. (2020)

Freezing

Freezing chicken carcasses is another way to reduce Campylobacter contamination (Georgsson et al., 2006; Harrison et al., 2013; Sampers et al., 2010). In one study, freezing treatment followed by 31 days of frozen storage at − 20 °C reduced the natural Campylobacter contamination level by 0.65–2.87 log CFU/1000 g in broilers (Georgsson et al., 2006). Freezing naturally contaminated chicken livers at − 25 °C for 24 h also reduced Campylobacter contamination levels by up to 2 log CFU/g (Harrison et al., 2013). Sampers et al., (2010) also reported that 1 day of frozen storage at − 22 °C reduced Campylobacter contamination by approximately 1 log CFU in both naturally contaminated chicken skin and minced chicken meat (Sampers et al., 2010). However, several studies have shown that prolonged frozen storage is not very effective at further reducing Campylobacter contamination (Eriksson et al., 2023; Georgsson et al., 2006; Sampers et al., 2010). Freezing temperature can affect the inactivation rate of Campylobacter (Zhao et al., 2003). When the inoculated chicken wings were stored at − 20 °C and − 86 °C for 52 weeks, C. jejuni was reduced by 4 and 0.5 log CFU/g, respectively (Zhao et al., 2003).

Surface cooling

In a study by Burfoot et al., (2016), spraying chicken carcasses with liquid nitrogen, which causes rapid surface cooling, was demonstrated to reduce Campylobacter contamination on chicken carcasses. Passage through the spraying tunnel for 40 s reduced Campylobacter on the breast skin samples by 0.9 to 1.5 log CFU/g on the day after treatment (Burfoot et al., 2016).

Sanitizers

Sanitizers such as sodium hypochlorite are commonly used to disinfect food materials and food processing environments in the food industry (Fukuzaki, 2006). However, chemical residues are a concern that often results in negative consumer perceptions (Table 1). Chlorine-based sanitizers are commonly used to reduce the microbial load on the surface of meat and poultry and to sanitize food contact surfaces because they are inexpensive and effective (Matthews et al., 2017). Previous studies have investigated the effect of chlorine-based sanitizers on Campylobacter contamination on the surface of meat samples (Table 3) (Bashor et al., 2004; Northcutt et al., 2005; Zhang et al., 2018). In one study, carcass washing with chlorinated water was shown to be effective at reducing Campylobacter, but it could not completely eliminate Campylobacter contamination (Bashor et al., 2004). A different study demonstrated that spray washing of broiler carcasses using chlorine was not effective against Campylobacter (Northcutt et al., 2005). In a recent study, however, the washing treatment of chicken thighs with acidified sodium hypochlorite at 225 ppm significantly decreased the naturally contaminating Campylobacter level and was more effective than the washing treatment using water or chlorine (8 ppm) (McWhorter et al., 2023).

Table 3.

Inactivation effects of sanitizers on Campylobacter in previous studies

Sanitizers	Mode of contamination	Objects	Conditions	Log reduction	References
Chlorinated water	Natural	Chicken carcasses	Pressurized washing at 25–35 ppm	0.5	Bashor et al. (2004)
Acidified sodium hypochlorite	Natural	Chicken thighs	Manual agitation for 10 s in the solution at 225 ppm	~ 1.6 compared to water wash	McWhorter et al. (2023)
Peracetic acid	Artificial	Skinless chicken breast meat	Immersion at 80 ppm for 30 min at 4 °C	0.5–0.8	Chen et al. (2020)
Peracetic acid	Artificial	Chicken breast fillet	Immersion at 100 ppm for 30 s	0.78	Kumar et al. (2020)
Peracetic acid	Artificial	Chicken breast fillet	Immersion at 1000 ppm for 30 s	1.9	Kumar et al. (2020)
Peracetic acid	Artificial	Chicken breast fillet	Spraying at 100 ppm for 5 s	0.34	Kumar et al. (2020)
Peracetic acid	Artificial	Chicken breast fillet	Spraying at 100 ppm for 5 s, then resting for 30 s	0.58	Kumar et al. (2020)
Peracetic acid	Artificial	Chicken breast fillet	Spraying at 1000 ppm for 5 s	1.43	Kumar et al. (2020)
Peracetic acid	Artificial	Chicken breast fillet	Spraying at 1000 ppm for 5 s, then resting for 30 s	1.63	Kumar et al. (2020)
Peracetic acid	Natural	Chicken carcasses	Manual agitation for 1 min in the solution at 200 ppm	1–2 compared to water wash	McWhorter et al. (2022)
Peracetic acid	Artificial	Chicken wings	Manual agitation (~ 150 rpm) for 30 s in the solution at 0.1%	2.5	Shen et al. (2019)
Cetylpyridinium chloride	Artificial	Broiler chicken parts	Rinsed at 0.35 and 0.60% for 23 s in a rotating decontamination tank of one rotation	4–5	Zhang et al. (2018)
Cetylpyridinium chloride	Artificial	Quail carcasses	Immersion with air agitation at 0.45% for 20 s	1.1 compared to water treatment	Rincon et al. (2020)
Chlorous acid	Artificial	Chicken juice	400 ppm for 3 min	> 8	Hatanaka et al. (2020)

Peracetic acid or peroxyacetic acid, the peroxide of acetic acid, is considered to be a safe, commercially-useful strong oxidant, disinfectant, and an effective sanitizer against Campylobacter contamination in poultry meat (Table 3) (Bogun et al., 2023; Chen et al., 2020; Chen et al., 2023a; Kitis, 2004; Kumar et al., 2020; McWhorter et al., 2022; Shen et al., 2019; Wideman et al., 2016). For example, spraying peracetic acid at 1200 ppm on artificially contaminated chicken drumstick skins led to a significant reduction in C. jejuni both immediately and during storage in modified atmosphere packages (30% CO₂, 70% O₂) (Rilana et al., 2019). When peracetic acid was applied to chicken breast meat under chilling conditions in an experiment mimicking chilling only or the scalding and chilling of commercial poultry processing, a significantly greater reduction in C. jejuni was detected, with a 0.5–0.8 log reduction compared to the same conditions without peracetic acid (Chen et al., 2020). In the study, susceptibility to peracetic acid was dependent on C. jejuni strains (Chen et al., 2020). In a different study, Campylobacter abundance in naturally contaminated chicken carcasses was significantly reduced after washing the carcasses with peracetic acid at 100 or 200 ppm, and this effect was similar to that of treatment with 50 ppm sodium hypochlorite (McWhorter et al., 2022).

Cetylpyridinium chloride, a quaternary ammonium compound, is an antimicrobial agent approved for poultry carcasses (Jiang and Xiong, 2015; Zhang et al., 2018). In one study, broiler carcass parts inoculated with Campylobacter were treated with several antimicrobials in a post-chill decontamination tank for 23 s, and the reduction effect was studied (Table 3) (Zhang et al., 2018). Cetylpyridinium chloride (0.35 or 0.60%) was the most effective treatment tested, with a reduction of 4–5 log CFU/sample, while treatment with peracetic acid (0.07 or 0.1%) resulted in a reduction of 1.5 log CFU/sample, and chlorine (0.003%) and acidified sodium chlorite (0.07%) resulted in reductions of less than 1 log CFU/sample (Zhang et al., 2018). Additionally, immersion of inoculated quail carcasses in cetylpyridinium chloride for 20 s resulted in a greater than 1 log CFU/mL reduction in C. coli (Table 3) (Rincon et al., 2020).

There have been several advances in the development of more effective sanitizers. Chlorous acid was more effective than sodium hypochlorite in the inactivation of Campylobacter in the presence of chicken juice (Table 3) (Hatanaka et al., 2020). Quaternary ammonium compounds with biscationic moieties performed better than the current commonly used quaternary ammonium compounds that have monocationic moieties such as benzalkonium chloride and cetyl pyridinium chloride (Gunther et al., 2018). Silver-stabilized hydrogen peroxide treatment by dipping or spraying reduced Campylobacter contamination levels in chicken wings by up to 2 log CFU/mL (Bourassa et al., 2021).

Organic acids

The use of organic acids is a common strategy for the decontamination of meat carcasses (Sofos et al., 2013). Organic acids are used to wash the surface of animal carcasses to reduce bacterial contamination in the United States (Beier et al., 2019). Organic acids are inexpensive, simple, and safe, but their antimicrobial effect is dependent on food pH (Table 1). It is commonly known that they enter microbial cells in an un-dissociated form, then dissociate under neutral pH inside the cells, leading to cell death (Birk et al., 2010; Davidson et al., 2013). However, a recent study showed that the dissociated forms of organic acids were more related to Campylobacter inhibition than the undissociated forms of organic acids (Beier et al., 2018; Beier et al., 2019). In addition, a recent study showed that organic acid-based agents can also reduce the surface adhesion ability of Campylobacter (Corcionivoschi et al., 2023). In the aforementioned study, they decreased the expression of the flaA gene, which is involved in bacterial motility, and changed the bacterial surface polysaccharides, which are related to the reduced ability of Campylobacter to attach to chicken carcasses (Corcionivoschi et al., 2023).

Several studies have demonstrated that organic acids are effective against Campylobacter on the surface of meat. Lactic acid, formic acid, citric acid, and tartaric acid are known to be effective against Campylobacter (Beier et al., 2018; Beier et al., 2019; Birk et al., 2010; Chaine et al., 2013; Cil et al., 2019; Riedel et al., 2009). In a previous study, C. jejuni was reduced by 1.6–1.7 log CFU when C. jejuni-contaminated chicken skin was dipped in lactic acid or formic acid for 1 min as opposed to a 1.0 log CFU reduction when the skin was dipped in sterile water (Riedel et al., 2009). C. jejuni decreased by 0.5 to 2 log CFU/meat after 2–10% tartaric acid was spread on the surface of chicken meat samples inoculated with C. jejuni (Birk et al., 2010). In one study, acetic acid, citric acid, and fumaric acid were compared for their ability to reduce C. jejuni on inoculated fresh chicken legs by dipping the chicken legs into the acids at 20 °C for 5 min (Gonzalez-Fandos et al., 2020). Of the three acids, citric acid was the most effective, with a reduction of 2.7 log CFU/g (Gonzalez-Fandos et al., 2020).

A recent study demonstrated that combined organic acids are more effective than a single organic acid against Campylobacter (Peh et al., 2020). For example, a combination of citric acid (0.02%), lactic acid (0.025%), and sodium dodecyl sulfate (0.0125%) reduced Campylobacter by 100% after 15 s of treatment (Bai et al., 2022). In the same study, increased concentrations of similar compounds (0.06% citric acid, 0.08% lactic acid, and 0.02% sodium dodecyl sulfate) reduced the isolation rate of Salmonella or Campylobacter from gloves and cutting tools in chicken slaughterhouses by 60–80% compared to that from none-treated samples (Bai et al., 2022).

Strain-to-strain variation in susceptibility to organic acids exists (Birk et al., 2010). When C. jejuni strains were exposed to 0.3% tartaric acid in brain heart infusion broth for 29 h, the abundance of the most resistant strain, 305A, decreased by only 1.59 log CFU/mL while that of the most sensitive strain, 327, decreased by 4.48 log CFU/mL (Birk et al., 2010).

Natural antimicrobials derived from plants

The interest in natural antimicrobials for food application has increased, which is consistent with consumers’ demands for healthier and safer food (Table 4). Natural compounds are promising alternatives to traditional antimicrobial agents, but their safety for human health needs to be proven (Table 1). Many natural compounds derived from plants have been shown to be effective against Campylobacter (Table 4). Like other foodborne pathogens, Campylobacter can be controlled by natural plant materials containing phenolic compounds, polyphenols, flavonoids, or terpenoids (Table 4). These active compounds include eugenol, thymol, limonene, carvacrol, 1,8-cineole, elemicin, linalool, citral, baicalein, and rosmarinic acid (Table 4). For example, clove bud oil inhibited the growth of Campylobacter at a concentration of 0.020%, and its main antimicrobial compound was eugenol (Navarro et al., 2015) (Table 4). In the same study, grapefruit essential oil at a concentration of 0.25% inhibited the growth of Campylobacter (Navarro et al., 2015). Grapefruit contains limonene, which is a monoterpene and the main antimicrobial compound of grapefruit essential oil. Cinnamon essential oil and its main antimicrobial agent, (E)-cinnamaldehyde, were effective against Campylobacter, and its minimum inhibitory concentration (MIC) was only 25–50 μg/mL for both C. jejuni and C. coli (Gahamanyi et al., 2020). Cardamom essential oil (Elettaria cardamomum (L.) Maton), derived from a traditional medicinal plant, inhibited the growth of both C. jejuni and C. coli at MIC of 0.025–0.050 μL/mL (Mutlu-Ingok et al., 2019). Cardamom essential oil’s main active compounds were α-terpinyl acetate and 1,8-cineole, which are terpenoids. Oregano essential oil (Origanum minutiflorum) is mainly composed of carvacrol, which is a phenolic monoterpenoid and is very effective against Campylobacter, with an MIC less than 1 mg/mL (Aslim and Yucel, 2008).

Table 4.

Plant-derived natural antimicrobials effective against Campylobacter

Common name (scientific name)	Active compounds	Application	Concentration (effective)	References
Alpinia katsumadai seed	Phenolic compounds	MHB	> 275 μg/mL	Kovač et al. (2014)
Anise myrtle (Syzygium anisatum)	Anethole	Nutrient broth	> 0.125% (v/v)	Navarro et al. (2015)
Blue gum (Eucalyptus globulus)	1,8-Cineole	Nutrient broth	> 0.2% (v/v)	Navarro et al. (2015)
Blue mallee (Eucalyptus polybractea)	1,8-Cineole	Nutrient broth	> 0.2% (v/v)	Navarro et al. (2015)
Cactus pear (Opuntia)	Phenolic compounds	MHAH/MHB	> 1 mg/mL	Sánchez et al. (2014)
Cardamom (Elettaria cardamomum Maton)	α-Terpinly acetate and 1,8-cineole	MHB	> 0.025 μL/mL	Mutlu-Ingok et al. (2019)
Carrot (Daucus carota L.)	(E)-methylisoeugenol and elemicin	MHA/MHB plus minimal eagle medium	> 125 μg/mL	Dedieu et al. (2020), Rossi et al. (2007)
Chinese chive (Allium tuberosum)	2-Amino-5-methylbenzoic acid	MHA	No MIC determined	Mnayer et al. (2014)
Cinnamon basil (Ocimum basilicum L.)	Phenolic compounds and flavonoids	MHB	> 220 μg equivalent chlorogenic acid/mL	Abramovič et al. (2018)
Cinnamon oil (Cinnamomum cassia(L.) J.Prl)	(E)-Cinnamaldehyde	MHAH/MHB	> 25 μg/mL	Gahamanyi et al. (2020)
Clove oil	Phenylpropene	Edible film	> 0.75%	Keawpeng et al. (2022)
Clove	Eugenol	Iso-Sensitest broth, chicken breast, beef, cherry tomato, and green grapes	> 0.6 mg/mL	Chen et al. (2023b)
Clove bud oil (Eugenia caryophyllate)	Eugenol	Nutrient broth	> 0.02% (v/v)	Navarro et al. (2015)
Coriander oil (Coriandrum sativum)	Linalool	BHI supplemented with 0.5% Tween 80, chicken, and beef	> 0.03% (v/w)	Rattanachaikunsopon and Phumkhachorn (2010)
		MHA/MHB	> 0.5 μL/mL	Duarte et al. (2016)
Cumin (Cuminum cyminum L.)	p-Mentha-1,3-dien-7-al, cumin aldehyde, γ-terpinene, and β-pinene	MHB	> 0.025 μL/mL	Mutlu-Ingok et al. (2019)
Dill weed (Anethum graveolens L.)	Carvone and limonene	MHB	> 0.012 μL/mL	Mutlu-Ingok et al. (2019)
Fennel (Foeniculum vulgare Mill.) seed	Polyphenols	MHB	> 2 mg/mL	Malin et al. (2022)
Garlic (Allium sativum)	Organosulfur compounds, allicin	Saline, nutrient broth	> 6 μg/mL	Lu et al. (2011)
		MHA	No MIC determined	Mnayer et al. (2014)
		Nutrient broth	> 0.05% (v/v)	Navarro et al. (2015)
Ginger oil	Phenolic compounds, eugenol, and shogaols	Chicken skin	> 0.25%	Wagle et al. (2021)
Grapefruit oil (Citrus paradisi)	Limonene	Nutrient broth	> 0.25% (v/v)	Navarro et al. (2015)
Hedyosmum strigosum Todzia	Thymol, α-phellandrene, thymol acetate, linalool	MHB supplemented with 5% horse serum	> 125 μg/mL	Cartuche et al. (2022)
Lavender flower (Lavandula angustifolia)	Linalool, linalyl acetate, and 1,8-cineol	MHB	> 0.2 mg/mL	Ramić et al. (2021)
Lemon (Citrus limonum)	Limonene	Nutrient broth	> 0.25% (v/v)	Navarro et al. (2015)
Lemon balm (Melissa officinalis L.)	Phenolic compounds	MHB	> 3.4 mg/mL	Mekinić et al. (2014)
Lemon grass (Cymbopogon citratus)	Citral	Nutrient broth	> 0.125% (v/v)	Navarro et al. (2015)
Lemon myrtle oil (Backhousia citriodora)	Citral	Nutrient broth	> 0.01%	Kurekci et al. (2013)
Lemon thyme (Thymus citriodorus)	Phenolic compounds, and flavonoids	MHB	> 280 μg equivalent chlorogenic acid/mL	Abramovič et al. (2018)
Lime (Citrus aurantifolia Christm.)	α-Terpineol, terpineol, and limonene	MHB, chicken	> 2 mg/mL	Valtierra-Rodríguez et al. (2010)
Mandarin (Citrus reticulata)	Limonene	Nutrient broth	> 0.25% (v/v)	Navarro et al. (2015)
Mastic oil (Pistacia lentiscus var. Chia)	Monoterpenes	BHI with soft agar	> 0.5% (v/v)	Gkogka et al. (2013)
Narrow-leaved peppermint (Eucalyptus radiata)	1,8-Cineole	Nutrient broth	> 0.1% (v/v)	Navarro et al. (2015)
Nettle leaves (Urtica dioica L.)	Phenolic compounds	MHAH/MHB	> 0.5 mg/mL	Garofulić et al. (2021)
Nettle-leaf mint (Meehania urticifolia)	Phenolic compounds	MHAH/MHB	> 400 μg/mL	Gahamanyi et al. (2020)
Niaouli (Melaleuca quinquenervia ct)	1,8-Cineole	Nutrient broth	> 0.1% (v/v)	Navarro et al. (2015)
Nopal cactus (Opuntia ficus-indica L.)	Flavonoids and polyphenols	BHIY	> 0.3 mg/mL	Castillo et al. (2011)
Olive oil (Olea europaea)	Phenolic compounds	MHA	No MIC determined	Dagdelen, (2016)
Oregano (Origanum vulgare L.)	Phenolic compounds	MHB	> 1.7 mg/mL	Mekinić et al. (2014)
Oregano oil (Origanum minutiflorum)	Carvacrol	MHB	> 7.8 μg/mL	Aslim and Yucel, (2008)
Pennyroyal (Mentha pulegium L.)	Piperitone	MHB	> 0.063% (v/v)	El Baaboua et al. (2022)
Peppermint (Mentha piperita L.)	Phenolic compounds	MHB	> 1.7 mg/mL	Mekinić et al. (2014)
Plum (Prunus L.)	Phenolic compounds	MHB	> 2 mg/mL	Valtierra-Rodríguez et al. (2010)
Rosemary (Rosmarinus officinalis L.)	Rosmarinic acid, carnosic acid, camphor, and 1,8-cineole	MHB	> 78 μg/mL	Klančnik et al. (2012)
		MHA	> 0.5%	Walid et al. (2022)
		MHB, chicken meat juice	> 0.08 mg/mL	Piskernik et al. (2011)
Sage (Salvia officinalis L.)	Phenolic compounds	MHB	> 0.82 mg/mL	Mekinić et al. (2014)
Skullcap (Scutellaria baicalensis Georgi)	Baicalein	MHAH/MHB	> 400 μg/mL	Gahamanyi et al. (2020)
Sorghum	Phenolic compounds	MHA	> 100 μg/mL	Schnur et al. (2021)
White sorghum	Phenolic compounds	MHA, chicken meat	> 6.25 mg/mL	Hamad et al. (2023)
Spearmint (Mentha spicata)	Carvone, limonene	Coatings on chicken	> 0.5%	Ala and Shahbazi (2019)
Stinkwort (Inula graveolens)	Monoterpene	MHB, chicken meat	> 0.2% (v/v)	Djenane et al. (2012)
Sweet acacia (Acacia farnesiana L.)	Flavonoids, polyphenols	BHIY	> 0.2 mg/mL	Castillo et al. (2011)
Tasmanian native pepper (Tasmannia lanceolata)	Eugenol	Nutrient broth	> 0.012% (v/v)	Navarro et al. (2015)
Tea tree oil (Melaleuca alternifolia)	Terpinen-4-ol	Nutrient broth	> 0.001%	Kurekci et al. (2013)
Thyme (Thymus serpyllum L.)	Phenolic compounds	MHB	> 3.4 mg/mL	Mekinić et al. (2014)
Thyme (Thymus vulgaris)	Thymol	Nutrient broth	> 0.006% (v/v)	Navarro et al. (2015)
Whitesage brush (Artemisia ludoviciana Nutt.)	Flavonoids and polyphenols	BHIY	> 0.5 mg/mL	Castillo et al. (2011)
Winter savory (Satureja montana)	Carvacrol, thymol, and thymoquinone	MHB	> 250 μg/mL	Šimunović et al. (2020)

MHB Mueller–Hinton broth, MHAH Mueller–Hinton agar supplemented with 5% defibrinated horse blood, MIC minimum inhibitory concentration, BHI brain heart infusion broth, BHIY BHI supplemented with 0.6% yeast extract

Organosulfur compounds commonly found in garlic such as allicin, allyl sulfide, and diallyl sulfides are another group of natural antimicrobial agents that are effective against Campylobacter (Bhatwalkar et al., 2021; Lu et al., 2011; Wagle et al., 2021). Lu et al. (2011) reported that the abundance of C. jejuni in 6.25 μL of garlic concentrate/mL saline decreased by 1 log after 24 h of storage at 4 °C, and a 2–3 log reduction occurred at garlic concentrations greater than 25 μL/mL under the same storage conditions. They also found that the antimicrobial effect of garlic due to organosulfur compounds was much greater than the effect due to phenolic compounds (Lu et al., 2011).

While most studies have tested the antimicrobial effects of natural antimicrobial agents in growth media, several studies have demonstrated promising results for the application of natural antimicrobial agents to chicken meat, chicken meat juice, and other food products (Hamad et al., 2023; Piskernik et al., 2011; Rattanachaikunsopon and Phumkhachorn, 2010) (Table 4). In one study, white sorghum extract was shown to be effective against C. jejuni in inoculated chicken fillets stored at 4 °C (Hamad et al., 2023). Treatment with white sorghum extract at concentrations of 2%, 4%, and 6% resulted in a full reduction of C. jejuni on inoculated chicken fillet samples on the 10th, 8th, and 6th days, respectively, during storage at 4 °C (Hamad et al., 2023). Dipping chicken meat samples in or mixing with Eleutherine americana bulb extract at 4–8 mg/mL was effective in reducing Campylobacter by more than 1 log CFU during 7 days of storage at 4 °C (Musthafa et al., 2021). Treatment of ground chicken meat and beef with 0.1–0.5% coriander oil also effectively inactivated C. jejuni in a dose-dependent manner during 3 h of storage at 4 or 32 °C (Rattanachaikunsopon and Phumkhachorn, 2010). Rosemary extract is another effective agent against C. jejuni, but its antimicrobial effect in chicken meat juice is reduced compared to that in a liquid medium, and at a higher level of C. jejuni contamination in chicken meat juice (Piskernik et al., 2011).

During the last decade, several food byproducts have been studied for their antimicrobial effects on Campylobacter and found to be promising cheap alternatives to current antimicrobial agents (Table 5). They contain high amounts of phenolic compounds and terpenes and include the seeds, peels, shells, or wastewater of plants such as berries, olives, chestnuts, grapes, pomegranates, and oranges (Table 5). However, most of these studies evaluated only the MIC, and additional studies are necessary for the application of these materials in food processing and preservation.

Table 5.

Food byproducts with antimicrobial effects against Campylobacter

Common name (scientific name)	Active compounds	Concentration (effective)	References
Blueberry and blackberry pomaces	Phenolic compounds	> 0.4 mg GAE/mL	Salaheen et al. (2014)
Chestnut inner shell (Castanea sativa)	Phenolic compounds and flavonoid	> 1 mg/mL	Lee et al. (2016)
Chirimoya leaves (Annona cherimola Mill.)	Germacrene D, sabinene, β-pinene, and bicyclogermacrene	> 500 μg/mL	Valarezo et al. (2022)
Grape vine leaves (Vitis vinifera L.)	Phenolic compounds, flavonoids, and stilbenes	> 0.7 mg GAE/mL	Katalinic et al. (2013)
Grape skin (Vitis vinifera)	Phenolic compounds, flavonoids, and catechins	> 0.014 mg GAE/mL	Katalinić et al. (2010)
Grape seed extract	Phenolic acids, catechins, and proanthocyanidins	> 20 μg GAE/mL	Silván et al. (2013)
Olive mill wastewater (cv. Cornicabra)	Phenolic compounds and secoiridoids	> 0.25 mg/mL	Silvan et al. (2019)
Pomegranate peel (Punica granatum)	Punicalagin and gallic acid	> 10 mg/mL	Skenderidis et al. (2019)
Sour orange peel (Citrus aurantium L.)	Limonene, linalool, p-coumaric acid, and ferulic acid	> 2 mg/mL	Valtierra-Rodríguez et al. (2010)
Soybean seed coat	Phenolic compounds	> 1%	Abutheraa et al. (2017)
Winemaking waste	Epicatechin gallate, resveratrol	> 40 μg GAE/mL	Mingo et al. (2016)

GAE gallic acid equivalent

Many studies have demonstrated that natural antimicrobial compounds from plants are more effective against Campylobacter than other microorganisms, such as Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes (Cartuche et al., 2022; Friedman et al., 2002; Haghighi et al., 2019; Katalinić et al., 2010; Kurekci et al., 2013; Mingo et al., 2016; Mutlu-Ingok et al., 2019; Schnur et al., 2021). This phenomenon may be due to the lack of a related efflux mechanism in C. jejuni (Dedieu et al., 2020). In one study, winemaking waste significantly reduced Campylobacter but did not affect lactic acid bacteria (Mingo et al., 2016). The phenolic compounds extracted from sorghum also exhibited an inhibitory effect on Campylobacter, while they had no effect on E. coli O157:H7 or S. Typhimurium (Schnur et al., 2021). In a study using Hedyosmum strigosum Todzia essential oil, C. jejuni had a much lower MIC (125 μg/mL) than other major pathogenic bacteria, such as E. coli (MIC of 2000 μg/mL), Salmonella enterica (MIC of 4000 μg/mL), and L. monocytogenes (MIC of > 4000 μg/mL) (Cartuche et al., 2022). In different studies, however, C. jejuni was more sensitive to commonly used essential oils or plant compounds, such as oregano, cinnamon, thyme, and eugenol, than other foodborne pathogens, E. coli O157:H7, S. enterica, and L. monocytogenes (Friedman et al., 2002; Haghighi et al., 2019). Grape skin extracts, especially white varieties, were more effective against C. coli than against other pathogenic bacteria, such as Bacillus cereus, Staphylococcus aureus, E. coli O157:H7, and Salmonella Infantis (Katalinić et al., 2010). In another study, C. jejuni and C. coli were more sensitive to tea tree oil, the essential oil derived from Melaleuca alternifolia, which is composed of monoterpenes and monoterpenoids such as α-terpinene and cineole, than other microorganisms such as B. cereus, E. coli, and S. Typhimurium (Kurekci et al., 2013).

Some studies have shown that different Campylobacter strains have varying degrees of susceptibility to natural antimicrobials such as oregano and winemaking waste (Aslim and Yucel, 2008; Mingo et al., 2016). The susceptibility of Campylobacter to oregano (O. minutiflorum) was highly strain-dependent, with MICs varying between 7.8 and 800 μg/mL (Aslim and Yucel, 2008). The MIC and minimal bactericidal concentration of winemaking waste extract against Campylobacter ranged between 40 and 160 mg gallic acid equivalent (GAE)/L and between 100 and 320 mg GAE/L, respectively, depending on the strain (Mingo et al., 2016).

For application in food products, recent studies have focused mainly on coating materials impregnated with antimicrobial compounds. Antimicrobial compounds are mixed with coating materials such as chitosan and gelatin, and food products are then coated with these antimicrobial films to extend shelf life and improve food safety (Pandey et al., 2023). In previous application studies, chicken samples were coated with antimicrobial films, and the viability of Campylobacter inoculated on chicken samples was studied during refrigerated storage (Ala and Shahbazi, 2019; Moller et al., 2022; Olaimat et al., 2014; Shrestha et al., 2019b; Wagle et al., 2019b). In these studies, natural antimicrobials such as eugenol, carvacrol, and allyl isothiocyanate were mixed with coating materials such as pectin, chitosan, gum arabic, and carrageenan. Significant reductions in Campylobacter abundance were observed after several days of refrigerated storage. For example, in one study, chicken breast fillets were inoculated with C. jejuni at 5 log CFU/g, coated with carboxymethyl cellulose coatings containing spearmint (Mentha spicata) and/or Ziziphora clinopodioides, and then stored under refrigerated conditions for 14 days (Ala and Shahbazi, 2019). In this study, C. jejuni was completely inactivated after 10 days of storage for the sample treated with the coating containing 0.5% Ziziphora clinopodioides + 0.5% Mentha spicata in contrast to less than a 1 log CFU/g reduction in the noncoated sample.

Nanotechnologies

Nanotechnology can also be used to enhance food safety, and antibacterial nanoparticles (NPs) can be used to control foodborne pathogens at various stages of the food supply chain. Some studies have evaluated the activity of nanoparticles against Campylobacter and have shown that silver (Ag), copper oxide, zinc oxide (ZnO) NPs, and titanium dioxide (TiO₂)-based nanocomposites exhibit effective antibacterial activity (Duffy et al., 2018; He et al., 2022; Noreen et al., 2019; Schneider et al., 2021). In particular, to prevent the emergence and spread of antibiotic-resistant Campylobacter, combination treatment with ZnO NPs and carvacrol, a natural antibacterial agent, has been confirmed to have a synergistic antibacterial effect that causes cell reduction of more than 6 log10 within 24 h (Windiasti et al., 2019). In this study, carvacrol induced damage to the outer cell membrane through the stress response of Campylobacter, and the study proposed a mechanism by which ZnO NPs promote cell structure destruction and the penetration of carvacrol. Additionally, antimicrobial surfaces embedded with antimicrobial NPs may reduce the risk of cross-contamination of food preparation surfaces. In one study, a diamond-shaped carbon nanocomposite embedded with Ag NPs was deposited on a silicon wafer to produce an antibacterial surface, and the antibacterial activity was measured (Zakarienė et al., 2018). As a result, the number of C. jejuni inoculated on the surface decreased by 4.06 log CFU/mL after 15 min.

The incorporation of nanotechnology into food packaging allows a variety of new approaches to improve food quality and safety. Absorbent pads functionalized with ZnO NPs have been designed to be introduced into food packaging to control C. jejuni without adding antibacterial agents directly to food (Hakeem et al., 2020). In contrast to the lack of a significant decrease in C. jejuni levels (~ 4 log₁₀ CFU/25 g) in the control group, C. jejuni levels in raw chickens stored on the absorbent pads decreased to undetectable levels (≤ 500 cells) after 5 days of storage at 4 °C. Chitosan film, a nontoxic polymer, can be used as a biodegradable food packaging material with antibacterial activity through the introduction of ozonated olive oil nanocapsules (Nowak et al., 2022). This environmentally friendly packaging material exhibits dual antibacterial activity due to chitosan and ozone, and induces growth inhibition of Campylobacter species in pork stored at 4 °C through the release of encapsulated ozone from the packaging material.

Another area for the application of nanotechnology is the nanostructuring of antibacterial agents. Accordingly, efforts have been made to prepare the natural antibacterial agents eugenol and carvacrol in nanoemulsion form to reduce C. jejuni in poultry after harvest (Shrestha et al., 2019a; Wagle et al., 2019a). However, in the case of eugenol and carvacrol, the improvement in antibacterial activity due to treatment in nanoemulsion form was not evident compared to the suspension treatment conditions. On the other hand, a strategy to encapsulate vegetable oils at the nanoscale using ucuuba butter and shea butter as nanostructured lipid carriers was effective (Ribeiro et al., 2021). In disc diffusion tests used to determine the in vitro antibacterial activity, the antibacterial activity of the nanocapsule formulations (35–43 mm) was found to be greater than that of the free oil (21–28 mm). The MICs of the nanocapsule formulation of olibanum essential oil was found to be 1.56 mg/mL and 0.78 mg/mL against free and sessile C. jejuni, respectively. Additionally, the use of nanocapsule formulations has positive effects, such as improving their physicochemical stability, solubility, and functionality and reducing their cytotoxicity, photodegradation, and volatility (Ribeiro et al., 2021).

Although nanotechnologies have high chemical and physical stability and a wide range of applications, the effects of human exposure are still poorly understood, and environmental release is another concern (Table 1).

Ultraviolet (UV) light

The emerging nonthermal technology of UV treatment, which operates in the wavelength range of 100 to 400 nm in the light spectrum, is widely used for the inactivation of microorganisms. It is easy to handle, inexpensive, and has a wide disinfection range but is inefficient for opaque liquid foods, or solid foods (Table 1). UV spectra can be categorized according to their wavelength ranges as UV-C (200–280 nm), UV-B (280–315 nm) and UV-A (315–400 nm), and UV-C has demonstrated the greatest bactericidal effects (Delorme et al., 2020). Applicability of UV-C light has been considered for its efficiency to control microbes which has direct and indirect effects on microbes (Byelashov and Sofos, 2009; Koutchma, 2019). Several important aspects of UV light make it promising for application in the meat production and processing chain, such as its ease of installation, lack of interruption of food production flow, lack of toxic byproducts, and its economic and environmentally friendly technology (Byelashov and Sofos, 2009; Koutchma, 2019). The most important advantage of UV light is the possibility of causing no change or only negligible changes in the physicochemical and sensory properties of food commodities, but this possibility depends mostly on UV-C parameters, food types and target microbial species (Bottino et al., 2017; Canto et al., 2019; Isohanni and Lyhs, 2009; Monteiro et al., 2017; Zhao et al., 2019). Several studies with different UV approaches have shown effective inactivation of Campylobacter spp. Moazzami et al. (2021) reported that 1 to 3 min of treatment with UV-C light-emitting diodes (LEDs) can effectively reduce C. jejuni on transport crates by 2.0 ± 0.5 to 3.1 ± 1.0 log CFU/mL of swab diluent (Moazzami et al., 2021). Haughton et al. (2012) reported that 1 or 5 min of treatment of skinless chicken fillets with high–intensity near ultraviolet/visible light (395 ± 5 nm) at 3 cm decreased the abundance of C. jejuni by 2.21 and 2.62 log CFU/g, respectively. Currently, some authors have shown the availability and effectiveness of mercury-free UV light technology as a low-cost device known as a UV-LED. This UV-LED device does not produce any toxic materials, as this technology uses semiconducting materials to produce radioactivity (Song et al., 2016). In a very recent study, it was shown that UV-LED exposure (at 280 nm) reduced CFUs by more than 1.62 log CFU/mL (Soro et al., 2023). This approach shows strain-dependent inactivation efficiency, where one of the eight strains shows high resistance (0.39 log CFU/mL) to UV light (Soro et al., 2023). The microbial inactivation mechanism of UV-C has been well explained in some articles showing that dimerization occurs in DNA, for instance, cyclobutane pyrimidine dimers (CPDs) and pyrimidine 6–4 pyrimidone photoproducts, which results in DNA damage to microbial cells. This damage hinders RNA transcription and DNA replication and disturbs normal cell function, causing cell death (Singh et al., 2021; Soro et al., 2023). Despite all the effective inactivation levels shown by various researchers, we cannot avoid the possibility of gaining the adaptive responses shown by some categories of stains towards specific types of UV light. Therefore, the efficiency of decontamination might decrease after repeated treatments with similar methods (Soro et al., 2021).

Control strategies during preparation

The handling of raw poultry is a high-risk factor for Campylobacter dissemination in kitchen environments (Humphrey et al., 2001). Food contact surfaces such as knives, cutting boards, and workers’ hands are frequently contaminated during poultry preparation (Eriksson et al., 2023; Lai et al., 2021; Lai et al., 2022). In addition, other sites, such as floors, are frequently contaminated (Lai et al., 2022). Contaminated surfaces can transfer Campylobacter to ready-to-eat foods, including fresh fruits and vegetables, through direct contact (Kusumaningrum et al., 2004; Luber et al., 2006). Therefore, the proper handling of poultry meat and timely and effective cleaning practices are critically important for preventing cross-contamination in the kitchen environment and preventing human infections (Bai et al., 2021; Eriksson et al., 2023; Lai et al., 2022). Although public education is always an important way to achieve good practices in kitchens (Bearth et al., 2013), some studies have demonstrated promising results in reducing Campylobacter cross-contamination in the kitchen environment (Thormar and Hilmarsson, 2010). Glycerol monocaprate reduced the levels of Campylobacter contaminating the surfaces of plastic and wooden boards by more than 2 log (Thormar and Hilmarsson, 2010). Antibacterial nanoparticles are also potentially useful for food contact surfaces in kitchen environments, as mentioned above (Zakarienė et al., 2018).

Conclusion

Many strategies have been studied and developed to control Campylobacter at the postharvest level. However, the current methods for inactivating Campylobacter contaminating poultry meat are still limited and not effective enough to substantially reduce human infections caused by Campylobacter. In addition, many studies have used inoculated food samples, while the inactivation of Campylobacter in naturally contaminated foods is more challenging. Recently, natural antimicrobial agents have been extensively studied, but many studies are still limited to evaluating the effectiveness of antimicrobial agents without applications in foods. Therefore, further studies are needed to develop more effective control methods for poultry meats as well as other food items. Because different control methods have different advantages and disadvantages, adequate methods must be chosen based on the conditions and situation (Table 1). It is also noteworthy to consider such a large strain-to-strain variation in resistance to some control methods (Aslim and Yucel, 2008; Birk et al., 2010; Chen et al., 2020; Soro et al., 2023). In addition, combined methods need to be further developed for more effective control of this important foodborne pathogen.

Declarations

Conflict of interest

On behalf of all authors, the corresponding author states that the authors declare no conflict of interest.