Abstract
Remarkable changes have occurred in poultry farming and meat processing in recent years, driven by advancements in breeding technology, feed processing technology, farming conditions, and management practices. The incorporation of probiotics, prebiotics, and phytoextracts has made significant contributions to the development of poultry meat products that promote both health and functionality throughout the growth phase and during meat processing.
Poultry fed with these substances improve meat quality, while incorporating probiotics, prebiotics, and phytoextracts in poultry processing, as additives or supplements, inhibits pathogens and offers health benefits to consumers. However, it is vital to assess the safety of functional fermented meat products containing these compounds and their potential effects on consumer health. Currently, there's still uncertainty in these aspects. Additionally, research on utilizing next-generation probiotic strains and synergistic combinations of probiotics and prebiotics in poultry meat products is in its early stages. Therefore, further investigation is required to gain a comprehensive understanding of the beneficial effects and safety considerations of these substances in poultry meat products in the future. This review offered a comprehensive overview of the applications of probiotics and prebiotics in poultry farming, focusing on their effects on nutrient utilization, growth efficiency, and gut health. Furthermore, potential of probiotics, prebiotics, and phytoextracts in enhancing poultry meat production was explored for improved health benefits and functionality, and possible issues associated with the use of these substances were discussed. Moreover, the conclusions drawn from this review and potential future perspectives in this field are presented.
Key words: poultry meat quality, probiotics, prebiotics, phytoextracts, functional fermented meat
GRAPHICAL ABSTRACT
INTRODUCTION
Due to the evolving perceptions of meat consumption and their increasing awareness of nutrition and health, the meat consumption market was currently undergoing a significant transformation (Kleyn and Ciacciariello, 2021). In 2023, global poultry meat production surpassed pork production by 17.61 million metric tons, reaching a total of 139.68 million metric tons (Figure 1). The poultry meat consumption market is experiencing rapid growth, projected to increase by 65% from 2015 to 2035, surpassing the growth rates of eggs (50%) and pork (35%) (Figure 2). Poultry meat, such as chicken, duck, and goose, fulfills the nutritional requirements of a contemporary healthy diet, characterized by being high in protein, low in calories, low in fat and low in cholesterol, and having a high digestive absorption rate (Wołoszyn et al., 2020; Goluch et al., 2023). However, the high protein and moisture content of poultry meat made it susceptible to spoilage and deterioration. This susceptibility was particularly evident during processing, storage, transport, and sales due to the high vulnerability of unsaturated fatty acids to oxidation and rotting (Katiyo et al., 2020). Consequently, the quality and nutritional value of the products decline while toxic and harmful substances may even be formed (Tsafrakidou et al., 2021).
Figure 1.
Production of meat worldwide from 2016 to 2023 (by type, in million metric tons).
Figure 2.
Percentage growth in demand for animal protein worldwide between 2015 and 2035 (by type, in percentage).
Probiotics can be used alone or in combination with other additives, generally regarded as safe (Biswas et al., 2023). Prebiotics are health-promoting substrates for microbes, encompassing fiber, polyphenols, polyunsaturated fatty acids, and conjugated linoleic acid (Peng et al., 2020; Biswas et al., 2023; Zhang et al., 2023). The incorporation of dietary probiotics, prebiotics and other beneficial substances can enhance the intestinal microbiota composition, augment the slaughter yield and ultimately elevate the quality of livestock and poultry meat (Vlaicu et al., 2020; Wang et al., 2018). When administered at effective dosages, these compounds have the potential to optimize the microbial equilibrium within the gastrointestinal system of poultry hosts, thereby enhancing digestion and promoting overall well-being, as well as protection against detrimental bacteria and pathogens (Jha et al., 2020). Moreover, a variety of approaches have been employed to reduce the fat content in poultry meat. These include the incorporation of microorganisms with probiotic functions (Bis-Souza et al., 2020), the utilization of plant extracts and compounds (Pérez-Burillo et al., 2019). These strategies not only contribute to minimizing the use of additives and ingredients associated with health disorders but also enhance the overall nutritional value of poultry products.
Probiotics, prebiotics, and phytoextracts significantly reduce antibiotic usage, enhance poultry meat quality, improve fat profile, prevent spoilage, extend the shelf life of fermented poultry products, and add health benefits to poultry meat (Chandra et al., 2021). Produced by probiotics, prebiotics, and phytoextracts, poultry and its meat products meet public demands for antibiotic-free meats and functional foods with extra benefits (Chowdhury et al., 2023). Aligned with the pursuit of a healthy lifestyle, these modifications can generally enhance public health by reducing the prevalence of chronic diseases like diabetes, obesity, fatty liver disease, and cardiovascular disease, as their lower fat content compared to conventionally produced poultry meat (Das et al., 2020). The significance of these researches lies in their potential to offer valuable insights for both poultry production and processing, thereby facilitating groundbreaking advancements in the field of poultry science.
This comprehensive review explores the diverse applications of probiotics, prebiotics, and phytoextracts in poultry farming, highlighting their pivotal role in enhancing nutrient absorption, improving growth efficiency, and promoting digestive health. Additionally, it illuminates the vast potential of these agents for producing wholesome and functional poultry meat products, underscoring their significance within the food industry. In addition, the challenges associated with implementing these substances in poultry farming, offering valuable insights into potential obstacles and strategies for overcoming them. It concludes by emphasizing the necessity for more comprehensive research and exploration of the full potential of these substances in poultry farming, with the ultimate objective of producing healthier and more sustainable poultry meat products for global markets.
FACTORS INFLUENCING THE QUALITY OF POULTRY MEAT
The quality of poultry meat and its related products can be influenced by various factors, which can be broadly categorized into 2 main processes: poultry rearing and meat processing (Figure 3). During the process of poultry rearing, the quality of poultry meat is significantly impacted by genetic, nutritional, and environmental factors (Baéza et al., 2022).
Figure 3.
Factors affecting poultry meat quality.
Factors Influencing the Quality of Poultry Meat During Rearing
The nutritional composition of the diet plays a crucial role in determining the quality of poultry meat. A well-balanced ratio of essential nutrients in the diet leads to enhanced nutrient utilization and superior overall quality (Jha et al., 2020). It is noteworthy that a negative correlation exists between the protein content in the feed and the proportion of fat in the live animal. This can be attributed to the increased energy demand for protein breakdown and reorganization, leading to reduced fat deposition (Liebert, 2017; Novodworski et al., 2023). Furthermore, the incorporation of additives into the diet has garnered recognition among numerous animal nutritionists for its profound impact on meat quality (Alagawany et al., 2020). The inclusion of vitamin E has been demonstrated to enhance the oxidative stability of poultry meat (Amevor et al., 2021) and found to increase the expression of matrix metalloproteinases (MMPs) within the muscle, increasing the proportion of soluble fiber in the muscle and promoting lipogenesis (Archile-Contreras et al., 2011). Additionally, vitamin D3 improves the water retention capacity of poultry muscles (Nong et al., 2023). Moreover, dietary calcium can reduce plasma cholesterol levels (Matuszewski et al., 2020), while yeast selenium supplementation can increase the micronutrient concentration in poultry meat (Markovic et al., 2018).
In addition to these factors, specific substances have been found to exert an influence on the quality of poultry meat as well. For instance, betaine serves as a source of active methyl groups for metabolic processes within the organism, thereby augmenting the levels of flavor precursors such as creatine, creatinine, inosinic acid, and myoglobin in poultry meat (Chen et al., 2022). The incorporation of chito-oligosaccharides in poultry diets has been demonstrated to ameliorate intestinal barrier damage, oxidative and immunological stress in lipopolysaccharide-challenged laying hens, as well as enhance the laying performance, egg quality, blood biochemistry, antioxidant capacity, and immune response in late-laying hens (Xu et al., 2020; Gu et al., 2022). The incorporation of citrus peel powder has been demonstrated to enhance the freshness, sweetness, and aroma of broth while effectively eliminating any undesirable flavors (Vlaicu et al., 2020). Additionally, polyphenols have been found to improve meat tenderness, juiciness, and flavor while reducing cholesterol content, thereby contributing to the production of high-quality chicken meat (Abdel Moneim et al., 2020).
Factors Influencing the Quality of Poultry Meat During Meat Processing
During the processing of poultry, various factors can impact the quality of poultry products. These factors encompass the techniques employed for slaughtering, transportation, storage, overall processing. The environmental conditions during storage play a critical role in determining the quality of poultry meat. Specifically, the storage temperature holds varying degrees of significance on the quality of poultry meat (Zelenakova et al., 2022). Generally, meat products demonstrate superior quality when stored at lower temperatures. Therefore, it is imperative to meticulously regulate the storage conditions and duration of poultry meat in order to ensure its optimal quality and flavor (Chen et al., 2020). Moreover, various techniques can be employed during poultry processing to sterilize the poultry and prolong its shelf life. These techniques encompass the utilization of preservatives, probiotics, prebiotics, phytoextracts, radiation, high-pressure treatment, and thermal treatment (Baéza et al., 2022; Lee et al., 2022).
EFFECTS OF ADDING PROBIOTICS AND PREBIOTICS TO FEED ON POULTRY MEAT QUALITY
Background of Applying Probiotic to Feeds
The growing demand for healthier diets and meats, particularly chicken meat, has resulted in a substantial surge in the production and consumption of poultry meat (Marangoni et al., 2015). In order to meet the growing market demand for meat and eggs, the poultry industry heavily relies on large-scale production of broilers and laying hens (Tenrisanna et al., 2023). The traditional practice involved confining broilers to indoor housing for their entire lifespan. However, in response to the public's growing preference for organic and locally sourced food, alternative management approaches have been explored (Ricke and Rothrock, 2020). A viable alternative in the poultry industry for antibiotics is the utilization of live probiotics, a natural feed additive that has garnered significant interest (Abd El-Ghany, 2020; Chowdhury et al., 2023). The primary objective of incorporating probiotics into poultry feed is to optimize and sustain poultry performance, while concurrently mitigating the risk of intestinal pathogen colonization and infection (Du et al., 2019). Furthermore, an increasing number of researchers suggest that using probiotics as dietary supplements holds great potential for improving the quality of poultry meat (Popov et al., 2021; Biswas et al., 2023).
Types of Probiotics in Feeds
The probiotic microorganisms commonly used in poultry feeds include Bacillus subtilis, Lactobacillus rhamnosus, Lactobacillus and Bifidobacterium rohita, Lactobacillus casei, Lactobacillus acidophilus, Lactobacillus coagulans, Escherichia coli, Lactobacillus lactis, Clostridium butyricum, Methanobacterium, and Streptococcus (Koshchaev et al., 2020; Mortada et al., 2020; Hassan et al., 2022). Certain Enterococci, particularly Enterococcus faecalis SF68 and Saccharomyces cerevisiae, have also been reported as being used in poultry feeds (Smialek et al., 2018). Furthermore, some studies have indicated that poultry can produce their own probiotics through rumen flora and intestinal flora.
Application of Probiotics in Poultry
Probiotics have emerged as a promising alternative to antibiotics in the poultry industry, offering not only enhanced growth rates but also reduced incidence of animal diseases (Nadhifah et al., 2020). Additionally, they exhibit inhibitory effects on foodborne pathogens (Forkus et al., 2017) and contribute to the improvement of poultry gut microbiota (Ramlucken et al., 2020). Moreover, it can contribute to environmental pollution reduction and overall food safety enhancement (Ricke and Rothrock, 2020).
Currently, the precise mechanism by which feed probiotics impact animal meat quality remains elusive. Given the intricate nature of the microbial community in the poultry gut, it is plausible that probiotics exert their effects through a multitude of mechanisms rather than a singular one (Yaqoob et al., 2022). The mechanisms of action associated with the addition of probiotics to poultry feed may encompass the optimization of gut flora composition, augmentation of intramuscular fat deposition, enhancement of organismal antioxidant capacity, and modulation of Ghrelin's endocrine hormones (Cox and Dalloul, 2015; Lokapirnasari et al., 2019; Shehata et al., 2022). The incorporation of probiotics into feed may exert substantial impacts on the poultry production environment (Alagawany et al., 2018). For a comprehensive understanding of the impacts of probiotic supplementation on poultry and its derived products, I would recommend referring to Figure 4, where these effects are succinctly summarized across 4 key aspects.
Figure 4.
The effect of dietary probiotics on poultry and its meat quality.
To the Environment
Poultry production contributes to phosphorus runoff due to the loss of effective phosphorus caused by phytates, which has led to a significant interest in the use of microbial phytase in the poultry industry for retaining available and effective phosphorus (Jha et al., 2020; Lamp and Moritz, 2022). Furthermore, the incorporation of probiotics into poultry diets has demonstrated efficacy in preventing the degradation of effective phosphorus by phytates (Abd El-Ghany, 2020). The incorporation of recombinant Lactobacillus cultures and calcium diets in poultry diets have been shown to enhance broiler weight gain, decrease production costs, and mitigate environmental impact (Li et al., 2018; Hu et al., 2021). Furthermore, in certain cases, the utilization of probiotic additives has resulted in a reduction of nitrogen levels in wastewater. This indicates enhanced feed efficiency and decreased nitrogen requirements in diet formulation, leading to reduced nitrogen leakage from the farm and its surrounding environment (Alagawany et al., 2018).
To the Poultry
Enhancement of Immunomodulation in Poultry
The utilization of probiotics not only enhances nitrogen and phosphorus absorption, thus reducing nutritional requirements, but also exerts potent immunomodulatory effects (Ma et al., 2018). Probiotics can effectively prevent poultry pathogen infections and enhance digestion and nutrient absorption in poultry by enhancing both innate and acquired immunity (Cox and Dalloul, 2015). Through research, it has been discovered that probiotics have the ability to enhance the expression of interferon gamma (IFN-γ) genes and significantly increase the secretion of IFN-γ protein in splenocytes of chickens immunized with the cpg adjuvant WIV H9N2 (Alqazlan et al., 2021). According to Swaggerty et al. (2019), modulating innate immunity by regulating macrophages, leukocytes, and b1-type lymphocytes has demonstrated superior efficacy compared to enhancing acquired immunity. However, further investigation is warranted to gain a more comprehensive understanding of these distinctions.
Maintaining the Balance of Intestinal Flora
Probiotics play a crucial role in maintaining the balance of intestinal flora. They achieve this by inhibiting the proliferation of pathogenic bacteria, thus effectively enhancing the growth and health of animals. Previous research done by Rodjan et al. (2018) revealed that the addition of probiotic into chicken's diet can significantly decrease the number of harmful microorganism Escherichia coli. Additionally, probiotics possess the capacity to mitigate the production of deleterious metabolites such as amines, ammonia, hydrogen sulfide, indole, and fecal odorants within the intestinal tract. This reduction in harmful substances exerts a positive influence on both gastrointestinal health and carcass quality, ultimately fostering enhanced broiler performance. Moreover, the utilization of probiotics also augments the gustatory excellence of poultry meat (Rodjan et al., 2018; Wu et al., 2019).
According to reports, the incorporation of 0.5% Bifidobacterium spp. + 0.25% Lactobacilli casei probiotics into diets has the potential to enhance the mucosal structure of the gastrointestinal tract, thereby inhibiting the proliferation of pathogenic bacteria and promoting egg production (Lokapirnasari et al., 2019). The probiotic strains Bifidobacterium, Lactobacillus, and Lactobacillus coagulans have demonstrated the ability to modulate the immune system, enhance metabolic processes, and restore intestinal flora homeostasis (Alqazlan et al., 2021; Shehata et al., 2022). Additionally, certain bacterial strains such as Bacillus subtilis and Bacillus licheniformis, Enterococcus faecalis, Lactobacillus acidophilus, and Bacillus glabrata, have been utilized as probiotics for the treatment of subclinical necrotizing enterocolitis (SNE) in poultry meat (Eeckhaut et al., 2016; Li et al., 2018; Sokale et al., 2019; Wu et al., 2019), as well as for inhibiting other foodborne pathogens commonly found in poultry products, including Escherichia coli, Staphylococcus aureus (El-Kholy et al., 2014), Yersinia pestis, Clostridium perfringens (Ramlucken et al., 2019), and Listeria monocytogenes (Olnood et al., 2015). The probiotic Lavipan, comprising Lactococcus lactis, Botrytis cinerea, Lactobacillus casei, Lactobacillus plantarum, and Saccharomyces cerevisiae, has demonstrated the ability to reduce Campylobacter invasion into the gastrointestinal tract of poultry under commercial production conditions. This reduction subsequently decreases the number of Campylobacter present in the gastrointestinal tract as well as the Campylobacter carcasses produced after processing (Smialek et al., 2018).
Enhancement of Nutrient Metabolism
The incorporation of probiotics, specifically lactic acid bacteria, into broiler feeds can significantly contribute to the reduction of cholesterol levels in poultry meat. The effectiveness of Bacillus coagulans in reducing both cholesterol and malondialdehyde content has been demonstrated by various studies (Popova, 2017; Majeed et al., 2019). Other research has reported positive effects of probiotics on broilers, including increased serum protein and albumin levels, as well as a decrease in total cholesterol and triglyceride levels in the blood (Yazhini et al., 2018). Additionally, supplementation with probiotics has been shown to reduce the cholesterol and fat content in both breast and thigh meat of broilers (Hossain et al., 2012).
Probiotics have demonstrated their ability to increase the content of inosinic acid, total amino acids, and fresh flavor amino acids in animal muscle, thereby enhancing the meat's flavor profile (Haščík et al., 2020), as well as facilitating lipid degradation reactions that generate volatile flavor components, thereby enhancing the overall taste profile of the meat (Purslow et al., 2012).Previous studies have demonstrated that the addition of 0.5 g/kg Bacillus subtilis to chicken feed can result in elevated levels of blood calcium and phosphorus, improved bone mass, enhanced brightness values in breast and leg muscles, elevated tethering force, as well as enhanced meat quality and flavor in broiler chickens (Mohammed et al., 2021).
Enhanced Tenderness of Poultry Meat
Probiotics possess the capacity to enhance the activity of superoxide dismutase, glutathione peroxidase, and other substances within the animal organism (Feng and Wang, 2020). Consequently, they effectively diminish the levels of reactive oxygen species (ROS). This reduction in ROS content plays a pivotal role in minimizing detrimental effects on muscle cell membranes containing phospholipids. As a result, it aids in preserving myoglobin freshness in fresh meat for an extended duration, leading to significant enhancements in meat color and reduced dripping loss (Bai et al., 2016; Xiang et al., 2019).
Multiple studies have indicated that the utilization of active Saccharomyces cerevisiae can enhance meat tenderness by increasing ghrelin and calcium levels in animal blood, as well as significantly elevating muscle calcium levels (Chang et al., 2019; Nidamanuri et al., 2021).The presence of calcium ions in muscle not only contributes to the regulation of calpain activity, but may also influence the type of muscle fiber, subsequently affecting meat tenderness (Huang et al., 2018). In simpler terms, the active Saccharomyces cerevisiae stimulates an increase in muscle calcium ion concentration induced by Ghrelin, thereby affecting various aspects such as muscle fiber type, calpain activity, and gene expression. As a result, this positively impacts meat tenderness and overall meat quality.
Addition of Prebiotics to Feeds
Prebiotics, when used as a dietary supplement, cannot be digested and absorbed by poultry. However, they can play a crucial role in promoting the selective growth of certain bacteria, improving intestinal microecology, and enhancing the absorption and utilization of nutrients (Peng et al., 2020). Researches indicated that the inclusion of prebiotics broiler diets leads to increased weight, yield, and fiber diameter in breast muscles. Furthermore, it results in higher levels of saturated fatty acids, polyunsaturated fatty acids, and n-3 fatty acids, while reducing redness values and monounsaturated fatty acid levels. These outcomes have a positive impact on human health (Tavaniello et al., 2018; Shehata et al., 2022).
The inclusion of 100 mg/kg chitosan in broiler diets has been proven to significantly enhance the antioxidant properties and meat quality of broilers, as well as improve the histological structure of intestinal mucosa and the composition of intestinal flora (Bami et al., 2021; Khajeh Bami et al., 2022). Supplementing poultry diets with tea polysaccharides has been proven to significantly enhance meat color, reduce drip loss, improve the antioxidant properties of poultry meat, and increase the content of muscle inosinic acid (Xie et al., 2020; Li et al., 2022). The inclusion of 0.5 g/kg quercetin to the diet of broiler chickens can increase the relative weight of the muscle, contribute to overall body health, and prolong the shelf life of meat by reducing lipid oxidation (Goliomytis et al., 2014). The addition of 20 mg/kg astaxanthin has been observed to enhance the chromaticity values (redness and yellowness) of broiler breast meat postslaughter, reduce cooking losses, significantly elevate the total free amino acids content in muscle, and improve the sensory evaluation of meat quality(Perenlei et al., 2014). The dietary supplementation of 0.75 g/kg hesperidin and 1.5 g/kg naringenin has exhibited positive effects on the antioxidant properties of chicken meat (Goliomytis et al., 2015). Furthermore, the administration of betaine at a dosage of 1,000 mg/kg has been observed to effectively mitigate oxidative stress in broilers and enhance chicken meat quality, particularly under conditions of heat stress (Wen et al., 2019). The evidence suggests that prebiotics have significant potential as essential additives in poultry rations to enhance the quality of poultry meat.
DEVELOPMENT OF FUNCTIONAL FERMENTED POULTRY MEAT PRODUCTS
Spoilage Microorganisms of Poultry Meat Products
The high moisture content, rich protein and essential nutrients, as well as the suitable pH value for microbial growth make fresh poultry meat highly susceptible to microbial contamination. Previous reports have identified the major spoilage bacteria in fresh poultry meat, including Pseudomonas aeruginosa, Bacillus immobilis, Bacillus thermophilus, Moraxella catarrhalis, Enterobacteriaceae, Lactobacillus, Corynebacterium albicans, Aspergillus spp., and others (Höll et al., 2016). The proliferation of these spoilage microorganisms resulted in the degradation of proteins and lipids in fresh poultry meat and its products, thereby adversely impacting the appearance, texture, and flavor of the final product (Iñiguez-Moreno et al., 2019; Kataria and Morey, 2020). The rapid growth of spoilage bacteria results in a relatively short shelf life of fresh poultry meat, typically lasting around 4 to 5 d. The presence of spoilage microorganisms significantly impacts the quality and safety of poultry meat, thereby exerting a profound influence on the development of the poultry market (Khalid et al., 2022) (Figure 5).
Figure 5.
SWOT evaluation of functional poultry meat products with probiotics.
Strengths
Fermentation is a Good Way to Preserve Meat Products
Fermentation is widely recognized as an effective method for increasing the shelf life of food by leveraging the actions of microorganisms and their metabolites (Kaveh et al., 2023). In meat fermentation, Lactobacillus, a commonly used bacterium, plays a pivotal role in reducing the pH level of the food and enhancing its sensory characteristics (Laranjo et al., 2017; Pannerchelvan et al., 2023). During the fermentation process, Lactobacillus strains play a vital role in acidifying the environment and producing various organic acids, such as lactic acid, acetic acid, hydrogen peroxide, and bacteriocins, through metabolic activities (Mathur et al., 2020; Petrova et al., 2022). The accumulation of organic acids during fermentation leads to a decrease in pH, which contributes to the breakdown of carbohydrates and ultimately improves the flavor, texture, and safety of the food product.
Studies have shown that Lactobacillus strains exhibit inhibitory effects on pathogenic bacteria, such as Salmonella and Listeria monocytogenes, in fermented meat. This inhibition contributes to slowing down lipid oxidation, thereby improving the product's quality and safety (Ben Slima et al., 2018). Brusa et al. conducted a study which revealed that Lactobacillus fermentation significantly reduces the risk of listeria pathogenic bacteria in fermented sausages by at least 3 orders of magnitude (Brusa et al., 2021). Importantly, the incorporation of Lactobacillus plantarum does not negatively impact the color and texture of the product. On the contrary, it enhances the viscoelastic and gelling characteristics of the samples (Zhu et al., 2020). Overall, the use of Lactobacillus plantarum strains offers a promising technique for producing higher-quality and healthier animal food products.
Various Strains Can Be Used in the Production of Functional Fermented Poultry Meat
Certain probiotics can effectively colonize meat products and provide health benefits both during the production of these functional fermented meat products and for human well-being. Table 1 provides a list of potential probiotics that can be used in the production of fermented poultry meat products. For instance, the utilization of probiotic in the treatment of chicken fillets resulted in a significant reduction in Staphylococcus aureus levels, thereby enhancing the microbiological properties and improving the physicochemical characteristics associated with yogurt-marinated chicken fillets (Masoumi et al., 2022). In another study, inoculating L. paracasei DTA 83 and S. boulardii 17 into chicken sausages and semifinished products exhibited inhibitory effects on the growth of various pathogens such as Pseudomonas aeruginosa, Acinetobacter baumannii, Escherichia coli, Staphylococcus aureus, and Klebsiella pneumoniae. These effects were attributed to the metabolites produced by these probiotics, including lactic acid and bacteriocins. Consequently, the shelf life of the products was extended (Almeida Godoy et al., 2022). The inoculation of L. plantarum into sucuk sausages resulted in the production of bacteriocin, which effectively inhibited the growth of Listeria monocytogenes (Kamiloğlu et al., 2019). The strains mentioned above fulfill the requirements for developing functionally fermented poultry meat products as they effectively colonize the meat throughout the processing phase. Moreover, their utilization has minimal impact on crucial meat quality parameters such as color, pH, oxidation state, textural features, and sensory attributes.
Table 1.
Probiotic or potentially probiotic used in meat products and the main results found in these studies.
| Product | Probiotic or potential probiotic used | Main results | References |
|---|---|---|---|
| Fermented sausage | L. rhamnosus CTC1679 (108 CFU/g) | Prevented the growth of Listeria monocytogenes (level <1 log CFU/g) throughout the whole ripening process and eliminated Salmonella. | Rubio et al. (2014) |
| Bovine meat | L. plantarum TN8 (108 CFU/g) | Inhibited the proliferation of spoilage microorganisms, such Listeria monocytogenes and Salmonella spp., delayed the lipid oxidation, improved texture parameters, and extended the shelf life of these products during storage. | Trabelsi et al. (2019) |
| Fresh pork sausage | L. sakei BAS0117 (105 CFU/g) | Inhibited the development of Salmonella Choleraesuis. | Gelinski et al. (2019) |
| Fermented pork sausage | L. rhamnosus LOCK900 (106 CFU/g) | Produced several bacteriostatic and bactericidal substances (e.g., lactic, acetic, formic acid, ethanol, or bacteriocin), thus inhibiting the development of spoiling and pathogenic microflora, including gram-negative strains belonging to the family Enterobacteriaceae and Pseudomonaceae and such species as Listeria monocytogenes, E. coli, or Staphylococcus aureus; thereby naturally preserving dry fermented meat products. Inhibited lipid oxidation in pork sausages. | Neffe-Skocińska et al. (2020) |
| Fermented sausage | E. faecium ATCC 8459 (109 CFU/g) | Inhibited the growth of coagulase-positive Staphylococcus, coliforms, and Salmonella spp. Rendered better sensory acceptance to the sausage. |
Carvalho et al. (2017) |
| Dry-fermented pork neck and sausage |
Bifidobacterium animalis subsp. lactis BB-12 (109 CFU/mL), L. rhamnosus LOCK900 (109 CFU/mL), L. acidophilus Bauer (109 CFU/mL) |
The 3 starter strains could be applied to smoked meat products. The culture L. acidophilus Bauer did not allow lipid oxidation and discoloration of the products. Sausage inoculated with L. acidophilus Bauer has the highest LAB count and a lower pH value. L. acidophilus Bauer preserved the quality of dry-fermented pork neck and sausage better than the Bif. animalis and L. rhamnosus LOCK0900, especially with regard to discoloration (higher CIE a* value, lower total color difference), lipid oxidation and lactic acid bacteria growth and survival. |
Wójciak et al. (2017) |
| Fermented sausage | L. sakei (108 CFU/g) | Strongly inhibited Escherichia coli ATCC25922, Salmonella Enteritidis ATCC13076, Vibrio parahaemolyticus, Staphylococcus aureus ATCC43300, Enterococcus faecalis ATCC29212, and Listeria monocytogenes CERELA | Mafra et al. (2021) |
| Dry fermented sausage |
L. rhamnosus R0011, L. rhamnosus Lr- 32, L. paracaseiLpc-37, L. casei Shirota, Enterococcus faecium MXVK29 (range: 106–108 CFU/g) |
They exhibited host stress-resistance, and halted the growth of E. coli, S. aureus, Candida spp., Listeria monocytogenes, and Salmonella choleraesuis. | Melo Pereira et al. (2018) |
| Salami |
L. plantarum 299v, L. plantarum DSM 9843, L. rhamnosus LbGG or ATCC 53103, L. casei Shirota YIT 9029, L. reuteri DSM 17938, L. casei ATCC 393 (106 CFU/mL) |
Reduced the abundance of spoilage bacteria, such as coagulase-positive staphylococci. Caused higher acidification and higher scores in taste parameters. Prolonged the shelf life. Improved the quality of salami. |
Blaiotta et al. (2018) |
| Tunisian dry fermented sausage | M. plantarum, S. xylosus (107 CFU/mL) |
L. plantarum improved the hygienic quality of fermented sausages by reducing counts of Enterobacteriaceae. Nitrate reductase activity of S. xylosus improved color of sausages with a more intensive red color. Both L. plantarum and S. xylosus improved sensorial characteristics of fermented sausage, and caused a significant decrease in pH as well as a significant increase in nitrite contents in inoculated sausages. |
Essid and Hassouna (2013) |
| Chicken fillets | L. casei 431 (108 CFU/mL) | Reduced microbial growth and improved the physicochemical quality of chicken fillets during storage and cooking time, via significantly decreasing the amount of Staphylococcus aureus, fecal coliforms, yeast and mold counts, pH index, malondialdehyde value, and cooking loss percentage in the experimental group, while increasing the water holding capacity. Improved the quality of chicken fillets. |
Masoumi et al. (2022) |
| Raw chicken sausages and semifinished chicken products | L. paracasei DTA 83, S. boulardii 17 (concentrations of 3.0%) | Exhibited good inhibitory effects on food-born pathogenic and spoilage microorganisms, such as Pseudomonas aeruginosa, Acinetobacter baumannii, Escherichia coli, Staphylococcus aureus, and Klebsiella pneumoniae. Presented good antimicrobial activity against various yeasts and molds. Extended the use-by date and improved meat quality. |
Almeida Godoy et al. (2022) |
| Pork-ham ready to eat packs | P. pentosaceus (106 CFU/mL) |
P. pentosaceus mediated production of bacteriocin-like substances and nisin, which helps in bringing about log 1.7 times inhibition of Listeria seeligeri. Lower weight loss and lipid peroxidation were observed in comparison with control samples. |
Azevedo et al. (2020) |
| Beef slices | C. maltaromaticum (108 CFU/cm2) | C. maltaromaticum mediated production of bateriocin, and it brought about marked reduction of Staphylococcus Typhimurium and E. coli. | Hu et al. (2019) |
| Sucuk sausages | L. plantarum (107 CFU/g) | L. plantarum mediated production of bacteriocin, which brings about a marked reduction in the growth of the Listeria monocytogenes. | Kamiloğlu et al. (2019) |
| Emulsion of goat meat | Murraya koenigii, P. pentosaceus (106 CFU/mL) | Murraya koenigii and P. pentosaceus mediated production of pediocin, and they can bring about 2- to 3-fold reduction in Listeria Innocua. | Kumar et al. (2017) |
| Salamitype sausage | Enterococcus faecium CRL 183 (109 CFU/mL) | Enterococcus faecium CRL 183 inoculated in a salami type sausage reduced lipid oxidation and did not affect the pH as well as Aw in relation to control sausage. | Roselino et al. (2017) |
| Fermented pork sausage | L. rhamnosus LOCK900 (106 CFU/g) | Inoculation of L. rhamnosus LOCK900 in fermented pork sausage led to significant reduction in Salmonella spp. and Listeria monocytogenes. | Neffe-Skocińska et al. (2020) |
The potential of Lactobacillus and Bacillus to produce antimicrobial metabolites makes them ideal candidates for natural preservatives in food safety. These metabolites have the ability to control the growth of spoilage and dangerous microorganisms in food (Liu et al., 2022). Particularly, the bacteriocins of metabolites exhibit enhanced thermal stability, broader pH tolerance, possess protein hydrolysis activity, and maintain effectiveness even at lower concentrations (Sadeghi et al., 2018; Faleh and Muzher, 2023). In general, the most common approach involves introducing bacteriocin-producing Lactobacillus cells as fermenters or protective cultures in fermented meat (Sonbol et al., 2020). Currently, a significant number of bacteriocin-producing strains of Lactobacillus and Bacillus have been isolated. However, there is still a strong worldwide interest in Lactobacilli bacteriocins, primarily due to their crucial role in food fermentation, flavor development, and food preservation, as well as their proven safety for human health (Moreno et al., 2018; Huang et al., 2021; Kaveh et al., 2023).
Weaknesses
The selection of an optimal probiotic starter for the production of functional meat products presents numerous challenges. This intricate process entails multiple stages and substantial costs, necessitating expertise in fields such as microbiology, food science, and medicine (Granato et al., 2020). In reality, only a limited number of probiotics meet these criteria. For example, in a recent study conducted on Ciauscolo salami, a traditional Italian fermented sausage, out of 42 isolated strains, only P. pentosaceus 62781-3, 46035-1, and 46035-4, as well as Mesenteria leuconostoc 14324-8, exhibited potential for use as probiotics in subsequent experiments (Federici et al., 2014). Similarly, an evaluation of E. faecalis strains in Sokobanja sausage identified only E. faecalis sk7-5, sk7-8, and sk9-15 as viable candidates for probiotics (Žugić Petrović et al., 2020). Furthermore, when selecting suitable probiotic strains, factors such as the expression of virulence genes, resistance to antibiotics, presence of biogenic amines and enterotoxins, as well as the synthesis of associated hazardous chemicals should all be taken into consideration. Two strains exhibiting β-hemolytic activity were identified in the studies conducted by Masalam et al. (2018) and Imane and Amel (2018), which aimed to identify potential probiotics from milk samples. Furthermore, the production of fermented meat products is a time-consuming and intricate process, often spanning several months or even years. This necessitates comprehensive evaluation through a range of tests encompassing color analysis, pH measurement, acidification rate assessment, water activity determination, hardness testing, cohesiveness examination, oxidation stability analysis, as well as sensory evaluation of the final product (Sidira et al., 2014; Roselino et al., 2017; Blaiotta et al., 2018; Song et al., 2018). However, it is generally observed that probiotics exhibit low thermal stability and their viability may be compromised during the heat treatment of meat products. This reduction in viability results in a decrease in the effective concentration of probiotics within consumers' gastrointestinal tracts (Terpou et al., 2019).
Opportunities
In recent years, the position of the poultry industry within the agricultural industry has significantly improved. Over the past 50 yr, the number of poultry farms has increased by approximately 5-fold (Mottet and Tempio, 2017). With the world's population expected to reach 9.3 billion people by 2050, there will be a substantial increase in both agricultural production and consumer demand, estimated to be nearly 60% higher than current levels (Falcon et al., 2022). There is a growing preference among individuals for poultry meat products such as sausages, jerky, and smoked meat. It is important to note that nitrates and nitrites are commonly used in sausages and smoked meats to enhance their sensory properties, oxidative stability, and microbiological safety. However, the presence of residual nitrite in meat can react with amines and amino acids, forming harmful nitrosamines that can adversely affect human health (Flores and Toldrá, 2021). Presently, consumers are increasingly aware of the impact of their diet on personal health and are actively seeking safer and healthier food options with higher quality, minimal processing, and fewer chemical additives.
The current trend in poultry products is to minimize the use of nitrates and nitrites. This has led to a growing interest in exploring natural antimicrobial compounds as alternatives to synthetic food additives (Nielsen et al., 2021). The application of probiotics in meat products is considered an appealing technique for enhancing the health benefits of meat (Pogorzelska-Nowicka et al., 2018). Through probiotic fermentation, beneficial compounds can be produced by breaking down polysaccharides, proteins, and fats in poultry meat, leading to the synthesis of bioactive compounds like peptides, organic acids, and conjugated linoleic acids (Kumar et al., 2017; Bis-Souza et al., 2020; Marco et al., 2021). Due to the nutritional characteristics of poultry meat, such as high protein and low fat content, it provides an optimal environment for promoting probiotic fermentation. This not only enhances the flavor of poultry products but also improves the survival rate of probiotics (Ursachi et al., 2020; Sirini et al., 2021). Therefore, incorporating probiotics and prebiotics into poultry meat products has emerged as a promising area of research in the development of functional animal products (Munekata et al., 2022). These functional ingredients not only enhance the safety and acceptability of poultry meat products but also offer a viable approach to reducing the usage of nitrates and nitrites while providing additional nutritional value. This can have a positive impact on human health and cater to the consumer demand for functional meat products with enhanced nutritional profiles (Sirini et al., 2021; Thøgersen and Bertram, 2021).
Threats
With an increasing awareness among consumers about the potential link between meat products and chronic diseases, the consumption of meat foods could potentially decrease (Cheah et al., 2020). Furthermore, the production of meat poses an additional threat due to its significant environmental implications. The rearing of animals for meat is a major contributor to environmental issues such as greenhouse gas emissions, water pollution, and overall degradation of the environment, all of which also have adverse effects on biodiversity (Hwang et al., 2020; Pinsard et al., 2023; Zhao et al., 2023).
Additionally, the probiotic market is currently dominated by the dairy industry, particularly with yogurt and fermented milk as its main products. This makes it challenging for probiotic-fermented meat products to establish a presence in the probiotic food market (Ávila et al., 2020). Finally, most fermented meat products, apart from fermented and dry-cured sausages, ham, and jerky, require heat treatment or cooking before being consumed. This heat treatment tends to reduce the number of viable probiotics present in the product, ultimately affecting their effectiveness in the gut (Pasqualin Cavalheiro et al., 2015). Therefore, exploring methods to increase the number of viable probiotics in fermented poultry products and ensuring their quality improvement is an important area for further investigation.
Prebiotic Functional Poultry Products
Prebiotics, as defined by ISAPP, are nondigestible food components that selectively serve as substrates for microorganisms (Swanson et al., 2020). When prebiotics and probiotics are combined in a single matrix, novel compounds are formed, offering the potential to maximize the effects of probiotics in prebiotic formulations (Cunningham et al., 2021). Among the most common prebiotics found in the diet are lactulose, oligogalactose (GOS), oligofructose (FOS), oligosaccharides (XOS), and inulin (Casarotti et al., 2018; Peng et al., 2020). The incorporation of prebiotics in meat products not only enhances their nutritional value but also influences the technical characteristics of various food items (Pogorzelska-Nowicka et al., 2018). A key area of focus in meat product research is the substitution of meat fat with beneficial additives like prebiotic dietary fiber (Das et al., 2020). Table 2 provides a list of some prebiotics and potential prebiotics suitable for use in meat products, while Table 3 showcases their potential synbiotic combinations with probiotics.
Table 2.
Prebiotics and potential prebiotics in meat products.
| Product | Prebiotic or potential prebiotic | Main results | References |
|---|---|---|---|
| Low-fat fermented sausage | Soy fiber (concentrations of 1 and 2%) | Presented a final fat reduction. Decreased the content of volatile compounds related to lipid oxidation. Increased the content of volatile compounds related to amino acids. |
Campagnol et al. (2013) |
| Reduced-fat Frankfurters sausage | Chia flour (concentrations of 5%) | Improved lipid profile and good fat content (lower saturated fatty acid, higher mono- and polyunsaturated fatty acid contents). Enhanced water binding properties. Created good stability to oxidation during storage. |
Pintado et al. (2016) |
| Dry fermented chicken sausage with fat reduction | Inulin Raftiline HP-Gel (concentrations of 7%) | Reduction of lipid content (52.9%). Higher titratable acidity, moisture and protein contents after ripening. Larger amount of soluble fibers. Improved its flavor and texture. |
Menegas et al. (2017) |
| Bologna sausage with fat reformulation | Chia flour (concentrations of 2.5%), Inulin (concentrations of 1%) | Enhanced fatty acid profile. (Higher amount of polyunsaturated fatty acids, increased the omega 3 content, and reduced saturated fat up to 41%) Affected the color of sausages, increasing L* and reducing a*. Created a more homogeneous and compact structure. Rendered the sausages greater hardness, chewiness, and shear force. Made the sausages healthier. |
Souza Paglarini et al. (2019) |
| Bologna sausage with phosphate reduction | Mucilage of chia (Hispanic Salvia L.) (concentrations of 2%) | The addition of 2% chia mucilage gel (MCG) proved a viable strategy to replace 50% phosphate in low-fat Bologna sausage. Provided better emulsion stability. |
Câmara et al. (2020) |
| Bologna sausage with reduced fat content | Oleogel rich in oleic acid (proportion of 1.5:1) | A good approach to fat replacement. Improved technological quality. Presented a better fatty acids profile. Increased emulsion stability and decreased cooking loss. Produced Bologna-type sausages with reduced fat, cholesterol, as well as energy value and with healthier lipid profile. |
Silva et al. (2019) |
| Low-fat Bologna sausage | Chia flour (concentrations of 10%) | A possible substitution for animal fats and phosphates. Provided better sensory acceptance and fatty acid profile. Resulted in improvements in the stability and texture parameters of the bolognas. |
Fernández-López et al. (2021) |
| Fermented sausage with low-saturated fat | Chia mucilage (concentrations of 5%) | Reduced pork back fat (PBF) and phosphate. Provided better stability to meat emulsion. Rendered sausages a less dense structure. Levels of polyunsaturated fatty acid increased by more than 56 %. Improved sensory acceptance. |
Ferreira Ignácio Câmara et al. (2021) |
| Bologna sausages with a reduction in fat content | Monoglyceride based-oleogels prepared from high oleic sunflower oils (concentrations of 5, 10, and 20%, respectively) | Monostearate-based oleogel provided a potential approach to fat replacement. Presented a better nutritional profile, with higher amount of unsaturated fatty acids. Reduced fat content and improved meat quality. Made the sausages lighter and a small increase in hardness. Enhanced the sliceability of the product. Rendered the product structure became more compact. Showed good acceptance by the consumers. |
Ferro et al. (2021) |
| Low-fat beef burger | Pineapple fibers (concentrations of 1.5%) | Improved cooking characteristics of the product, with higher water and fat retention and lower cooking loss and diameter reduction. Rendered the meat become harder, chewier, and more cohesive. Improved sensory characteristics of the product. |
Selani et al. (2016) |
| Low-fat burgers | Hydro-cold chia emulsion (concentrations of 12.5%) and linseed oils (concentrations of 12.5%) | Reduced the lipid content and improved the fatty acid profile of the burgers with a healthier n-6/n-3 PUFA ratio. Increased the hardness. |
Heck et al. (2019) |
Table 3.
Potential synbiotic meat products.
| Product | Potential synbiotic used | Main results | References |
|---|---|---|---|
| Low-fat fermented sausage | 2% Fructooligosaccharides (FOS) + L. paracasei BGP1, or 2% Fructooligosaccharides (FOS) + L. rhamnosus GG | Resulted in a significant decrease in fat content. Reductions in Enterobacteriaceae and yeast were observed. Had positive effects on the texture and safety of the sausage. |
Bis-Souza et al. (2020) |
| Salami | 2% Citrus fiber Citri-Fi + L. rhamnosus, or 2% Inulin Orafti HPX + L. rhamnosus, or 2% Arabinogalactan + L. rhamnosus | Increased antioxidant capacity of salami. Increased antioxidant capacity of metabolites released during fermentation by gut microbiota. Increased short chain fatty acids production. Helped shape gut microbial community structure. Deduced the prevalence of members of Escherichia and Shigella. |
Pérez-Burillo et al. (2019) |
| Dry-fermented sausage (Longaniza de Pascua) | 3% Chestnut flour + 8.5 log CFU/g L. plantarum Bioflora | Chestnut flour improved LAB counts. Chestnut flour not only had a significant effect on pH decrease and residual nitrite values, but also provided dietary fiber and polyphenols to the product. Produced greater amounts of lactic acid, and created a barrier in order to control undesirable microbiota. Improved the texture and changed the flavor of the product. The symbiotic meat product was successfully accepted by consumers, and it is considered a healthy matrix as a probiotic carrier. |
Sirini et al. (2020) |
| Low-fat Italian type salami | 2% Fructooligosaccharides (FOS) + L. casei SJRP66, or 2% Fructooligosaccharides (FOS) + L. casei SJRP169 | Proved to be useful to obtain a healthier meat product. The addition of FOS showed a positive effect on the L. casei viability. Decreased moisture content during the ripening time, which leads to a darker product. Increased hardness and chewiness. Improved sensory characteristics, product stability and safety. |
Bis-Souza et al. (2020) |
| Sausage | 1% Cactus pear peel flour + E. faecium UAM1, or 1% apple flour + E. faecium UAM1 | Presented higher lactic acid bacteria populations. Created fewer coliforms in the inoculated samples. Increased antioxidant capacity, and decreased the oxidative rancidity of lipids during storage. |
Barragán Martínez et al. (2020) |
In a study by Bis-Souza et al. (2020), oligofructose (FOS) and probiotic microorganisms such as Lactobacillus paracasei and Lactobacillus rehmannii were utilized as partial substitutes for pig back fat. The findings revealed a significant reduction in the fat content of the meat products in the group that underwent fat replacement compared to the control group without any fat substitution. Additionally, the inclusion of inulin as a fat substitute and probiotic bacteria had a significant impact on the texture of beef products. Hardness, stickiness, and chewiness increased significantly with maturation (Berizi et al., 2017; Jackson et al., 2023). During fermentation, the drop in pH leads to structural changes and aggregation of myofibrillar protein, which affects the rheological characteristics after dry fermentation (Montoya et al., 2022).
Furthermore, the combination of multiple prebiotics and probiotics has synergistic effects. Inulin and oligofructose promote the growth of Bifidobacteria, resulting in a decrease in pH, a reduction in the number of pathogenic microorganisms, and a decrease in the production of toxic metabolites (Xiudong et al., 2016). Okara, a by-product of soybean water extract, is rich in fiber and protein and can contribute to the fermentation of various meat products (Echeverria et al., 2022). A study investigated the effects of citrus fiber, inulin, and arabinogalactan on the formation of short-chain fatty acids during the in vitro digestion of Italian salami with Lactobacillus rhamnosus as a probiotic fermenter. The findings demonstrated that the addition of dietary fiber enhanced antioxidant capacity and synthesis of short-chain fatty acids, while reducing the presence of Escherichia coli and Shigella spp. during the fermentation process in the human gut flora (Pérez-Burillo et al.,2019). Moreover, Lactobacillus acidophilus and L. rhamnosus can enhance the acidity of meat products, which helps improve organoleptic characteristics such as firmness, taste, and color. These probiotics prevent the development of biogenic amines, inhibit pathogen growth, and mitigate the negative effects of lipids and proteins in these products (Wójciak et al., 2017).
Phytoextracts Functional Meat Products
In recent years, there has been extensive research on the antibacterial properties of various plant-derived extracts. Researchers have primarily focused on understanding the bioactivity principles of these extracts and their ability to enhance the performance and prolong the shelf life of meat products (Amiri and Rajabi, 2022; Deshmukh and Gaikwad, 2022). These plant bioactives contain specific amino acid sequences that are associated with health benefits, making them crucial for incorporating into meat products (Montesano et al., 2020). One promising research direction is exploring the combined use of plant bioactives and probiotic strains in meat products to develop new and healthier functionalities (Pérez-Burillo et al., 2019; Sirini et al., 2020).
Spices and herbal extracts commonly used in food products have garnered significant attention. Plant extracts can be utilized alone or in combination with other extracts, requiring minimal processing, to achieve synergistic effects in meat and meat products. Recent studies have demonstrated that clove and cinnamon oils (Adhikari et al., 2021; Feng et al., 2022), thyme and balsam oils (Fratianni et al., 2010; Altınterim and Kocabaş, 2017), as well as hops extracts (Kramer et al., 2015; Arruda et al., 2021) exhibit excellent inhibitory effects against meat spoilage bacteria. Plant extracts are generally recognized as safe (GRAS) and are preferred by most consumers over synthetic preservatives. However, it is important to note that the antimicrobial effectiveness of plant extracts can be influenced by meat characteristics and processing conditions (Amiri and Rajabi, 2022).
Hurdle Technology
Hurdle technology (HT) is a food preservation technique that influences the microbiological stability of food products by forming a protective barrier against spoilage and deterioration through the synergistic or interactive effects of various hurdle factors (Khan et al., 2017). Hurdle factors (HF) with preservative functions disrupt the microbial equilibrium of one or more microorganisms, preventing their growth, reproduction, and even rendering them inactive or dead (Aaliya et al., 2021). The main hurdle factors include temperature, pH, water activity (Aw), oxygen reduction value (Eh), pressure, irradiation, competitive flora, preservatives, as well as microwave sterilization and high-voltage electric field pulses (Luong et al., 2022). Combining naturally antimicrobial substances with nonthermal processing methods is particularly appealing, as this hurdle technology can effectively preserve the biological activity of these compounds while meeting the preservation standards for most foods (Peng et al., 2020; Bigi et al., 2023).
Currently, many commercially available meat products are produced using a combination of hurdle factors, such as irradiation, reduced water activity, and vacuum packaging (Khalid et al., 2022; Osaili et al., 2023). These compounds exhibit bactericidal action during processing, preventing postprocessing microbial contamination, reducing foodborne pathogens and harmful microorganisms, and extending the shelf life of meat products (Khan et al., 2017). Due to the high protein, moisture, and fat content of poultry meat, fresh poultry is prone to microbial growth and lipid oxidation (Domínguez et al., 2019). Several strategies exist to prevent microbial growth and slow down lipid oxidation, ensuring the quality and safety of poultry meat. Some of these methods include artificial drying (Agafonychev et al., 2021), vacuum packaging (Osaili et al., 2023), gamma irradiation (Khalid et al., 2022), high-pressure treatment (Jackowska-Tracz and Tracz, 2015), the use of chemicals (Silva et al., 2021; Ji et al., 2023), and the utilization of antimicrobial metabolites derived from fermenting microorganisms (Abouloifa et al., 2022; Lahiri et al., 2022).
CONCLUSIONS AND PROSPECT
This review provides a comprehensive overview of the application of probiotics and prebiotics in poultry production, with a focus on their pivotal roles in nutrient metabolism, developmental performance, and gastrointestinal health of poultry. Additionally, it explores the potential utilization of probiotics, prebiotics, and phytoextracts for the production of wholesome and functional poultry meat products while discussing associated concerns. These studies have convincingly demonstrated that incorporating probiotics, prebiotics, and plant extracts into poultry feed exerts a significant impact on the generation of healthy, sustainable, and nutritious meat products throughout both rearing and processing stages. The inclusion of these substances in poultry feed rations enhances the quality of poultry meat while effectively preventing the proliferation of putrefying bacteria in processed poultry meat through additives or packaged supplements derived from them.
Although current studies have yielded promising technical results and satisfactory organoleptic acceptability, further research is still needed to fully comprehend the metabolic mechanisms of poultry after being fed with probiotics and prebiotics, as well as the specific effects of these substances on meat products. Moreover, there is a significant knowledge gap concerning the safety of functional fermented meat products containing these substances and their impact on consumer health. Additionally, there is a limited body of research investigating the utilization of next-generation probiotic strains and probiotic-prebiotic synergists in poultry meat products, necessitating further in-depth research to acquire an extensive understanding of their health benefits and safety when incorporated into poultry meat products. Furthermore, exploring the combination of probiotics, prebiotics, and phytoextracts with other hurdle technologies such as vacuum and high pressure would offer potential benefits. Additionally, investigating the synergistic effects of probiotics and prebiotics during poultry meat fermentation is worthwhile.
ACKNOWLEDGMENTS
This work was financially supported by National Natural Science Youth Fund of China (32302107), Guangdong Province college youth innovative talent project (2023KQNCX010), and Guangdong seed industry revitalization project (2022-WPY-00-008).
Author Contributions: Sashuang Dong: Designed the framework, wrote and modified the manuscript; Lanyin Li: Collected data, wrote the manuscript and made drawings; Fanyu Hao: Organized literature and created tables; Ziying Fang: Summarized the literature and revised the chart; Ruimin Zhong: Revised the manuscript; Jianfeng Wu: Reviewed and polished full manuscript; Xiang Fang: Reviewed and edited the manuscript and provided funding for the acquisition.
Diagrams were created with Biorender (https://www.biorender.com/).
DISCLOSURES
The authors have no conflicts of interest.
Footnotes
Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.psj.2023.103287.
Contributor Information
Jianfeng Wu, Email: jianfeng.wu@scau.edu.cn.
Xiang Fang, Email: fxiang@scau.edu.cn.
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