Review Article

Growth Performance and Meat Attributes of Poultry in Response to Dietary Probiotic Supplementation: A Review

Teedzai Chitura*

Department of Animal Science, University of Venda, Private Bag X5050, Thohoyandou 0950 , South Africa.

Received | January 25, 2023; Accepted | March 20, 2023; Published | March 20, 2024

*Correspondence | Teedzai Chitura, Department of Animal Science, University of Venda, Private Bag X5050, Thohoyandou 0950 , South Africa.; Email: teedzai.chitura@ul.ac.za

Citation | Teedzai Chitura (2024). Growth performance and meat attributes of poultry in response to dietary probiotic supplementation: A review. Adv. Anim. Vet. Sci., 12(5):977-985.

DOI | https://dx.doi.org/10.17582/journal.aavs/2024/12.5.977.985

ISSN (Online) | 2307-8316

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Poultry products contribute to global food security as well as address the challenges of malnutrition faced by many marginalized households in developing countries (WHO, 2018). However, the expansion of poultry industries is threatened by factors such as a lack of improved chicken breeds, low planes of nutrition, and the high occurrence of diseases (Malematja et al., 2022). Over the years, antibiotic growth promoters have found use in poultry production for optimal gut health, reducing the effects of pathogens as well as enhancing growth performances (Sapsuha et al., 2021; Malematja et al., 2023). However, negative effects on human health due to the emergence of drug-resistance microorganisms are associated with the indiscriminate application of antibiotics in poultry farming (WHO, 2018; Peralta-Sánchez et al., 2019). In light of these challenges, alternative production systems that limit reliance on antibiotics are being explored. Probiotics are alternatives for improving gut health (Ricke and Rothrock, 2020) and optimal growth performance in birds (Krysiak et al., 2021) which according to Peralta-Sánchez et al. (2019) are the key attributes that alternatives to antibiotics should have. World Health Organization (2018) defined probiotics as living microorganisms supplemented to livestock to modulate gut health and maintain intestinal microflora colonizing the gut and subsequently improving performance of the host animal. Krysiak et al. (2021) defined probiotics as universal feed additives that can be incorporated into poultry diets with other feed additives. Probiotics are usually produced in the feed industry laboratories through the process of isolating and selecting desired microorganisms, cultivating, and fermenting, and used as feed additives in manufacturing feeds (Zhang et al., 2021).

Though there are many probiotic species registered for use in animal feeds, species such Lactobacillus, Lactococcus, Saccharomyces, and Bifidobacterium are commonly used in poultry feeds (Jha et al., 2020). Probiotics advance the growth performance by modulating the microbial community of the gut, hence promoting the development of the gastrointestinal tract and enhancing the overall health and performance of the bird (Malematja et al., 2022). The context of probiotic supplementation in livestock production is widely investigated. Several bodies of literature have reported enormous benefits of probiotic supplementation in poultry production, including improved gut health and general health condition, enhanced growth performance through improved feed conversion ratio, increase in growth rate and weight gain, and a reduction in mortality rates (Zhang et al., 2016, 2021). Some studies reported positive effects of probiotics in poultry production including their beneficial effects on carcass composition (Getabalew et al., 2020). Yang et al. (2010) reported improved tenderness when the probiotic C. butyricum was included in a diet. Furthermore, Peralta- Sánchez et al. (2019) reported increased egg production in hens supplemented with probiotics. Bacteria are popular probiotic microorganisms used in poultry production (Peralta-Sánchez et al., 2019). Although probiotics have proven to be effective in replacing prescribed antibiotic growth promoters in feeds, previous studies recommended further investigations on comparative studies, recommended dosages and methods of administration, and optimal ages for probiotic supplementation. The present review provides an overview of the application of probiotics in poultry production as antibiotic alternatives for improving the growth performance of birds and ensuring that poultry products are free from antibiotic residues and therefore safe for human consumption.

Literature search strategy

The literature search was conducted by accessing data from electronic database sources such as the Directory of Open Access Journals (DOAJ), Research Gate, Science Direct, Scopus, and Google Scholar. This review mainly focuses on the potential of probiotics in substituting synthetic growth promoters in poultry production in the context of an increasingly global human population that places a huge demand for poultry and other animal products. Furthermore, the search process was extended to cover the role played by probiotic supplementations on growth performance and meat quality in poultry production systems. Databases were accessed using several keywords which were paraphrased in different search engines. The keywords alternative growth promoter, antibiotics, meat quality, natural growth promoter, poultry, and probiotics were used in the search engines.

Challenges associated with the use of antibiotics and the potential use of probiotics in poultry production

Poultry meat has unsaturated fatty acids, oleic acid, and linoleic acids which reduce cholesterol as well as lower lipoproteins which are not desirable as they threaten human health (Zhang et al., 2021). Given these positive attributes, poultry industries are rapidly expanding along with the rising demand for poultry meat (Ghosh et al., 2019). The indiscriminate use of antibiotics as growth promoters in poultry production leads to serious consequences such as antimicrobial resistance in animals and drug residues in poultry products (Figure 1) which threatens global food safety and security (Zhang et al., 2021). As a result, the European Union (livestock production under Council Regulation (EC) No 2821/98) and several similar other organizations legislated and imposed restrictions on the use of antibiotics as growth promoters in animal feeds (Laxminarayan et al., 2015; Salim et al., 2018). Consequently, there is an upsurge in interest in selecting alternative growth promoters as a replacement for synthetic growth promoters (Krysiak et al., 2021; Zhang et al., 2021). Poonam and Srivastav et al. (2021) reported that the search for alternative growth promoters led to the identification of bacterial strains as a replacement for antibiotic growth promoters due to their desirable properties. The use of probiotics has proven to be important in improving the immune response thereby improving the overall performance of the host animal (Figure 1). Peralta-Sánchez et al. (2019) reported that since the discovery of the positive effects of probiotics in livestock production decades ago, bacterial species similar to those already existing in the gut of animals found common use in improving gut health and conditions by modulating intestinal microbiota. Some explanations were brought forward on how probiotics can influence gut health, animal welfare, and growth performances of the host animals (Figure 1). According to Salim et al. (2018), as antimicrobial agents, probiotics reduce pathogenic microbes population in the gut, aiding the digestion of feed. The second mechanism proposed by the same authors is that of modulation of the immune system response through elevated antibody titers. Krysiak et al. (2021) cited the mechanism of competitive exclusion, which involves the formation of a mucus attachment on the intestinal epithelial layer.

 

Probiotics are among the most effective methods of microbial control with no harm to the environment (Hejdysz et al., 2012). Multiple works of literature have proven in many ways that the use of probiotics has diverse benefits to the poultry meat industry and thus the prospect of using probiotics in poultry production is gathering momentum worldwide. However, the efficiency of probiotics vary with the species used and practical applications (Salim et al., 2018).

Utilization of probiotics in free-range and pasture-based poultry production systems

Natural poultry-rearing systems are gaining popularity as chickens are raised on organic feeds, which are preferred by a growing population of consumers globally (Shi et al., 2019). Natural rearing systems can either be free-range or pasture-based. Ricke and Rothrock (2020) cited some of the concerns regarding natural poultry rearing systems such as increased exposure of chickens to various pathogenic organisms and the fact that the birds have to rely solely on their natural defense mechanisms to combat pathogens. The same authors also indicated that the risk of salmonellosis is high in natural rearing systems. Exposure to harsh environments, provision of low-quality feedstuffs, and high mortality rates are some of the challenges of natural poultry rearing systems. According to Shi et al. (2019), given these challenges, the use of feed additives such as organic acids, medicinal oil extracts, probiotics, and prebiotics becomes key to ensure healthy and productive chicken flocks. Ricke and Rothrock (2020) observed improved growth performance and egg production following the use of probiotics while Khan and Chousalkar (2021) observed that probiotics could be used to control foodborne pathogens and ensure food safety. El-Jeni et al. (2021) reported that administration of probiotics to day-old-chicks could improve health conditions of free-range chickens by limiting the proliferation of foodborne pathogens as well as the colonization of the gut by pathogens thereby preventing the occurrence of diseases that threaten the health and production performance of free-range or pasture-raised chicken flocks.

Application of probiotics as a managerial tool for growth performance in large-scale or intensive production systems

Factors such as as genetic make-up, age, nutrition, health condtion, and sex have a significant effect on the growth performance of an animal (Al-Shawi et al., 2020). Gut microbial populations also play a crucial role by aiding the process of digestion and immune system development (Zhang et al., 2011). A balanced proportion between the beneficial and harmful microbial populations enhances nutrient digestibility resulting in improved growth performance (Jerzsele et al., 2012). Maintaining and stabilizing poultry gut conditions in large-scale productions with probiotics is inevitable (Atela et al., 2019). Colonization of the digestive tract with probiotics could induce nutrient utilization, which could result in improved growth traits of the host animal (Qorbanpour et al., 2018; Zhang et al., 2021). Furthermore, probiotic administration is said to modulate the gut microbial community and improve physiological responses and thus, improving the growth performance of chickens (Atela et al., 2019). Probiotic strains such as Lactobacillus are suitable for domestic animals as they inhibit the growth of pathogenic microbes while promoting the growth of beneficial microbes (Zhang et al., 2021). Administering probiotics in chicken’s diet improves feed utilization, thus improving feed intake, and feed conversion ratio, which could improve the overall growth performance, meat quality as well as egg production and quality (Getabalew et al., 2020). Zhang et al. (2016) reported positive effects on body weights, average daily gains, and nutrient digestibility in Cobb 500 broiler chickens fed diets with probiotics. Similarly, Alkhalf et al. (2010) made positive findings on the effects of supplementing probiotics in the diet on the growth performance of broiler chicks during the starter period. Ritzi et al. (2016) observed that probiotic supplementation in drinking water improved body weights in broiler chicks. Zhang et al. (2011) reported no effect on growth performance traits throughout the growth period. Contrary to these findings, Qorbanpour et al. (2018) investigated the effect of probiotic supplementation and observed no effect on weight gain and feed conversion efficiency in chickens. Similarly, Atela et al. (2019) reported that the administration of a multi-strain probiotic to indigenous chickens did not affect average weekly feed intake and weight gain. Findings on the effects of probiotic supplementation in poultry feeds are presented in Table 1.

 

Table 1: Effects of including probiotics in poultry diets on growth performance.

Probiotic strain	Administration or dosage	Host	Outcomes	Authors
Commercial product (Bacillus ssp.)	Direct fed provided in distilled water at 5.0 x 106 cfu of DFM suspended in 0.5 mL	Broilers	Did not affect body weight during the starter and grower phase	Lee et al. (2010)
Clostridium butyricum	Supplemented in the diet at 1×109 cfu/kg	Arbor acres	Dietary treatment did not influence growth performance in chickens at 20 and 40 days.	Zhang et al. (2011)
Bacillus licheniformis.	Provided in drinking water at a dosage rate of 1.1x1010 cfu/ml	Broilers	Improved body weight during the grower phase while feed conversion ratio was improved throughout the experimental period.	Liu et al. (2012)
Pediococcus acidilactici,, Enterococcus faecium, Bacillus subtilis, Lactococcus lactis, and Pediococcus pentosaceus	Provided in drinking water at B.109 cfu/l	Japanese quail	Administration of probiotics increased body weight at 42 days.	Bazrafshan et al. (2012)
Multi-species (Lactobacillus fermentum and Saccharomyces cerevisiae)	Incorporated in diets at 0.2 or 1% probiotic product (containing 1 × 107 cfu/g of Lactobacillus fermentum JS and 2 × 106cfu/g of Saccharomyces cerevisiae)	Cobb broilers	Dietary treatment improved feed intake (43.5 and 43.2 g/bird/day), feed conversion ratio (1.31 and 1.33 g: g), average daily gains (33.2 and 32.6 g/bird/day), and live weights (743,2 and 731,1 g/bird) of broiler chicks during the starter phase. The dietary treatment did not affect growth performances during the grower phase.	Bai et al. (2013)
Lactobacillus retuteri	Direct fed probiotics mixed with standard diet at 0.1%	Male Ross 308 broilers	Improved feed conversion ratios (0.74 g: g) and body weights (202 g per bird) during the starter phase and body weight (892 g per bird) during the grower phase. However, feed intake was not affected throughout the experimental period.	Salim et al. (2013)
Mixture of Lactobacillus retuteri, Bacillus subtilis, and Saccharomyces cerevisiae	Direct fed probiotics mixed with standard diet at 0.1%	Male Ross 308 broilers	Improved body weights during the starter (205 g per bird) and grower (895 g per bird) periods, however, the dietary treatment did not affect overall feed intake and feed conversion ratios.	Salim et al. (2013)
Lactobacillus strains (Lactobacillus johnsonii, Lactobacillus)	Provided in standard diet	Cobb broilers	Did not improve growth performance of chickens raised in cages.	Olnood et al. (2015)
Pediococcus acidilactici	Supplemented in basal diet at 0.8, 1 or 1.6 g/kg of feed	Broilers	Improved body weights and daily weight gains during grower phase. Similarly, feed conversion ratio was improved with no mortalities throughout the experimental period.	Alkhalf et al. (2016)
Commercial probiotics (PoultryStar®)	Probiotics provided in drinking water at 20 mg/bird per day	Male Cobb 500 broilers	Improved body weights during the starter phase. However, feed intake and feed conversion ratios were not influenced by probiotic supplementation.	Ritzi et al. (2016)
Clostridium butyricum	Supplemented in the diet at 2 × 107 cfu/kg of feed	Male Cobb broilers	Did not affect body weight and average daily gain during the starter period.	Zhang et al. (2016)
			Table continued on next page..............
Probiotic strain	Administration or dosage	Host	Outcomes	Authors
Bacillus subtilis	Provided in the diet at 200 or 400 mg/kg containing 4×109 33 cfu/g of probiotics	Ross 308 broilers	Feed intake, feed conversion ratios, and weekly body weights of broiler chickens were not affected by the dietary treatment.	Fathi et al. (2017)
Vitafor (Bacillus subtilis)	Administered in drinking water at 0.5 ml (107 cfu/g) per kg of live weight.	Goslings	Significantly improved daily weight average gains (47.5g) and live weights (3085.4g).	Khaziakhmetov et al. (2018)
Vitafor (Bacillus subtilis)	Administered in drinking water at 0.5 ml (107 cfu/g) per kg of live weight.	Broad breasted white turkey	Improved live weights (2659.5g) as well as daily weight gain (6.2g) of the birds compared to the control at 42 days.	Khaziakhmetov et al. (2018)
Lactobifadol (L. acidophilu and Bifidobacterium adolescentis)	Provided in the diet at a dose of 0.2 g probiotics/g per kg of live weight	Broad breasted white turkey	Improved live weights (2743.5g) and growth rate (63.9g) at 42 days.	Khaziakhmetov et al. (2018)
Lactobacillus (Commercial strains)	Probiotics provided in the diet at 1 g/kg of feed	Cobb 500	Did not affect the production performance of broilers throughout the production period.	Al-Khalaifa et al. (2019)
Bacillus tequilensis	Supplemented in the diet at at 200 g/ton DM.	Ross 308	Significantly improved feed conversion ratios (1.7 g: g) and improved body weight gains (2675.4g) of broiler chickens.	Hosseini et al. (2019)
Bacillus tequilensis	Supplemented in the diet at at 200 g/ton DM.	Ross 308 broilers	Dietary treatment did not affect feed intake throughout the production period.	Hosseini et al. (2019)
Combination of Bacillus subtilis and Bacillus licheniformis	Probiotics provided in the diet at 250g /100kg of feed	Broilers	Improved growth performance with respect to feed conversion ratios, daily weight gains, and live weights during the grower phase.	Roy and Khatun (2020)

 

Carcass quality and sensory attributes of meat from chickens fed dietary probiotics

Meat quality is an important aspect, which drives consumer purchasing decisions and consumption (Al-Shawi et al., 2020). Meat quality includes meat color, tenderness or texture, and water-holding capacity (Khan et al., 2018). These characteristics are influenced throughout the stages of life of an animal (Al-Shawi et al., 2020). There is widespread agreement among researchers that probiotic supplementation could improve the meat quality of broilers (Zhang et al., 2021; Mohammed et al., 2021). Hidayat et al. (2016) and Khan et al. (2018) indicated dietary supplementation of bacteria-based substances improves meat quality and sensory properties in both male and female birds. Tenderness, which is an important attribute of meat quality, is positively affected by probiotic supplementation (Krysiak et al., 2021). Studies have shown that probiotics have a positive effect on the quality aspects of both fresh and processed meat products (Trabelsi et al., 2019; Bis-Souza et al., 2020). Such effects include improvement in product quality and safety, extending shelf life (Kumar et al., 2017), imparting unique sensory qualities (Rouhi et al., 2018), and providing health benefits (Kumar et al., 2017). Park et al. (2016) observed improved meat tenderness and shear force in broiler chickens fed a Clostridium butyricum based probiotic. Current reports on the effects of probiotics on the sensory attributes of poultry meat are contradicting. For instance, some studies reported a positive influence of probiotics on poultry meat sensory properties while other studies reported no influence. Studies reported a positive effect of probiotics such as Bacillus licheniformis and Bacillus subtilis on the flavor of broiler meat (Liu et al., 2012; Mohammed et al., 2021). Some studies reported that the chemical properties of meat are among the factors positively affected by probiotics supplementation. According to Jadhav et al. (2015) and Aziz et al. (2020), supplementation of probiotics in poultry diets results in increased muscle and organ composition and an overall increase in carcass weight depending on the composition and inclusion levels of the probiotic given. It was reported that the protein composition of thigh and breast meat increased following probiotic supplementation. Duskaev et al. (2020) reported that probiotics increase amounts of chemical elements in the liver depending on the composition and concentration of the probiotic administered. Ali and Abdelaziz (2018) incorporated 0.160 g and 0.175 probiotic/liter of drinking water and observed increased water absorption in pectoral and femoral muscles, while concentrations of 0.175 g probiotic/liter of drinking water gave opposite results. The decrease in shear force was positively correlated with increased muscular fat content (Yang et al., 2010). In addition, the application of probiotics in broiler diets modulates the fatty acid composition of the meat through increased omega-3 fatty acids concentration such as eicosapentaenoic acid and docosahexaenoic acid. Improved protein efficiency ratio may may improve carcass yield at

 

Table 2: Effects of supplementing probiotics on poultry meat quality and sensory attributes.

Probiotic strain	Application or dosage	Host	Outcomes	Author
Bacillus tequilensis	Provided in the diet at 200 g/ton of feed.	Ross 308 broiler chickens	Increased carcass yield (67.4%), breast-meat (23.4%), thigh (16.8%), and spleen weight (0.2%) compared to the control group. However, probiotic supplementation did not affect the relative weight of the liver, gizzard, and heart of the birds. The abdominal fat was negatively affected (1.3%).	Hosseini et al. (2019)
Combination of Bacillus subtilis a Bacillus licheniformis	Probiotics provided in the diet at 250 g/100 kg of feed.	Cobb 500 Broiler chickens	Did not affect dressing percentage, thigh, and wing weights. However, improved meat quality with respect to breast meat and drumstick meat. Abdominal fat deposition was reduced.	Roy and Khatun (2020)
Bacillus subtilis	Probiotic provided in the diet at 0.25 g/kg of feed.	Ross 708 broiler chickens	Affected meat Ph and colour. Meat pH in the leg-muscle was reduced by the dietary treatment.	Mohammed et al. (2021)
Bacillus subtilis	Probiotic provided in the diet at 0.25 g/kg of feed.	Ross 708 broiler chickens	Increased meat colour in terms of the lightness, redness, and yellowness of leg meat.	Mohammed et al. (2021)
Bacillus subtilis	Probiotic provided in the diet at 0.5 or 0.25 g/kg of feed.	Ross 708 broiler chickens	Improved meat tenderness, flavor, juiciness, and texture. Supplementing probiotics increased the water holding capacity of leg meat, regardless of the supplementation levels compared to the control group.	Mohammed et al. (2021)
Bacillus tequilensis	Provided in the diet at 200 g/ton of feed.	Ross 308 broiler chickens	Improved carcass yields (67.4%), breast-meat (23.4%), thigh (16.8%), and spleen weights (0.2%) compared to the control group. However, probiotic supplementation did not affect the relative weights of the liver, gizzard, and heart of the birds. Abdominal fat was negatively affected (1.3%).	Hosseini et al. (2019)

 

slaughter age (Hossain et al., 2012). The carcass quality of broiler chicken meat is improved by probiotics dietary inclusion (Hosseini et al., 2019). Findings on the effects of probiotic supplementation on poultry meat quality and sensory attributes are presented in Table 2.

Limitations of using probiotics in poultry production

Though probiotics are regarded as an alternative growth promoter with many benefits in terms of health and growth performance. The efficacy of probiotics in improving the host’s performance and product quality hinges on factors such as probiotic strain being used as well as stability during storage, supplementation method, frequency and dosage, breed, sex, age, and health status of the host animal (Al-Shawi et al., 2020). Furthermore, probiotic products are fragile, and inadequate handling or conservation after acquisition may inactivate them (Bahule and Silva, 2021). Some literatures have demonstrated that the use of probiotics may pose a threat to the host animal’s defense mechanisms (Milner et al., 2021). It has been documented that an overdose of probiotics can lead to the deterioration of semen and possibly lead to infertility in breeders (Krysiak et al., 2021). Therefore, proper dosages are recommended when using probiotics in roosters.

Conclusions and Recommendations

Recently, there has been an increase in the demand for the production of organic foods and drug residue-free animals by international health organizations in order to meet human health standards. Based on this review, it can be concluded that probiotics and prebiotics were developed in order to reduce inappropriate application and mismanagement of antibiotics in poultry production, which have negative health effects on human health. Therefore, the present study reviewed the application of probiotics in place of antibiotics as growth promoters in chickens. Evidence from peer-reviewed and published manuscripts have shown that activities from livestock production are the major drivers of drug resistance. Following restrictions on antibiotic use, the use of probiotics has become popular. Overall search results have indicated that probiotics could be safely used in commercial poultry feeds to improve chicken productivity, improve meat quality, as well as meat acceptability. However, the choice of probiotic strain to be utilized, and application method or dosage will depend on the bird parameters or meat attributes that are being targeted. More studies are recommended to ascertain the findings reported in this review.

Acknowledgment

The authors would like to thank the University of Limpopo for assisting with resources to conduct this study.

Novelty Statement

The study explored the response in performance and meat attributes after probiotic supplementation in poultry.

Ethics approval

This study requires no ethics.

Conflict of interest

The authors have declared no conflict of interest.

References

Ali N, Abdelaziz M (2018). Effect of feed restriction with supplementation of probiotic with enzymes preparation on performance, carcass characteristics and economic traits of broiler chickens during finisher period. Egypt. J. Nutr. Feeds, 21: 243-225. https://doi.org/10.21608/ejnf.2018.75460

Al-Khalaifa H, Al-Nasser A, Al-Surayee T, Al-Kandari S, Al-Enzi N, Al-Sharrah T, Ragheb G, Al-Qalaf S Mohammed A (2019). Effect of dietary probiotics and prebiotics on the performance of broiler chickens. Poult. Sci., 98(10): 4465-4479. https://doi.org/10.3382/ps/pez282

Alkhalf A, Alhaj M, Al-Homidan I (2010). Influence of probiotic supplementation on blood parameters and growth performance in broiler chickens. Saudi J. Soil. Sci., 17(3): 219-225. https://doi.org/10.1016/j.sjbs.2010.04.005

Al-Shawi SG, Dang DS, Yousif AY, Al-Younis ZK, Najm TA Matarneh SK (2020). The potential use of probiotics to improve animal health, efficiency, and meat quality: A review. Agriculture, 10(10): 452. https://doi.org/10.3390/agriculture10100452

Atela JA, Mlambo V, Mnisi CM (2019). A multi-strain probiotic administered via drinking water enhances feed conversion efficiency and meat quality traits in indigenous chickens. Anim. Nutr., 5(2): 179-184. https://doi.org/10.1016/j.aninu.2018.08.002

Aziz NH, Khidhir ZK, Hama ZO, Mustafa NA (2020). Influence of probiotic (Miaclost) supplementation on carcass yield, chemical composition and meat quality of broiler chick. J. Anim. Poult. Prod., 11: 9–12. https://doi.org/10.21608/jappmu.2020.77767

Bahule CE, Silva TNS (2021). Probiotics as a promising additive in broiler feed: Advances and limitations. In: Advances in poultry nutrition research. Intech Open. Advances in Poultry Nutrition Research - Google Books.

Bai SP, Wu AM, Ding XM, Lei Y, Bai J, Zhang KY, Chio JS (2013). Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poult. Sci., 92(3): 663-670. https://doi.org/10.3382/ps.2012-02813

Bazrafshan K, Karimi TMA, Rahimi S (2012). Effect of some isolated bacteria from commercial probiotics on growth, carcass composition and immune system of Japanese Quail. Anim. Sci. J., 3(96): 15-24. https://www.sid.ir/paper/215079/en#downloadbottom

Bis-Souza CV, Penna ALB, da Silva Barretto AC (2020). Applicability of potentially probiotic Lactobacillus casei in low-fat Italian type salami with added fructooligosaccharides: In vitro screening and technological evaluation. Meat Sci,. 168: 108186. https://doi.org/10.1016/j.meatsci.2020.108186

Duskaev G, Rakhmatullin S, Kvan O (2020). Effects of Bacillus cereus and coumarin on growth performance, blood biochemical parameters, and meat quality in broilers. Vet. World, 13: 2484. https://doi.org/10.14202/vetworld.2020.2484-2492

El-Jeni R, Dittoe DK, Olson EG, Lourenco J, Corcionivoschi N, Ricke SC, Callaway TR (2021). Probiotics and potential applications for alternative poultry production systems. Poult. Sci., 100(7): 101156. https://doi.org/10.1016/j.psj.2021.101156

Fathi MM, Ebeid TA, Al-Homidan I, Soliman NK, Abou-Emera OK (2017). Influence of probiotic supplementation on immune response in broilers raised under hot climate. Br. Poult. Sci., 58(5): 512-516. https://doi.org/10.1080/00071668.2017.1332405

Getabalew M, Alemneh T, Zewdie D (2020). Overview on probiotics and their impact in commercial poultry production. Microbiol. Res. Int., 8(2): 43-50.

Ghosh SK, Bupasha ZB, Nine H, Sen A, Ahad A, Sarker MS (2019). Antibiotic resistance of Escherichia coli isolated from captive Bengal tigers at Safari parks in Bangladesh. J. Adv. Vet. Anim. Res., 6: 341-345. https://doi.org/10.5455/javar.2019.f352

Hejdysz M, Wiaz M, Józefiak D, Kaczmarek S, Rutkowski A (2012). The use of selected organic acids and their mixtures in the feeding of fattening chickens. Sci. Ann. Pol. Soc. Anim. Prod., 8(2): 59-68. (Google Scholar).

Hidayat MN, Malaka R, Agustina L, Pakiding W (2016). Abdominal fat percentage and carcass quality of broiler given probiotics Bacillus spp. Metabolism, 22: 3-60. (Google Scholar).

Hossain ME, Kim GM, Lee SK, Yang CJ (2012). Growth performance, meat yield, oxidative stability, and Fatty Acid composition of meat from broilers fed diets supplemented with a medicinal plant and probiotics. Asian-Aust. J. Anim Sci., (8): 1159-1168. https://doi.org/10.5713/ajas.2012.12090

Hosseini NG, Modarressi, MH, Mousavi SN, Ebrahimi MT (2019). Effects of indigenous spore-forming probiotic as feed supplement on performance and safety in broilers. J. Hell. Vet. Med. Soc., 70(4): 1841-1850. https://doi.org/10.12681/jhvms.22234

Jadhav K, Sharma KS, Katoch S, Sharma VK, Mane BG (2015). Probiotics in broiler poultry feeds: A review. J. Anim. Nutr. Physiol., 1: 4-16. (Google Scholar).

Jerzsele A, Szeker K, Csizinszky R, Gere E, Jakab C, Mallo J, Galfi P (2012). Efficacy of protected sodium butyrate, a protected blend of essential oils, their combination and Bacillus amyloliquefaciens spore suspention against artificially induced necrotic enteritis in broilers. Poult. Sci., 91(4): 837-843. https://doi.org/10.3382/ps.2011-01853

Jha R, Das R, Oak S, Mishra P (2020). Probiotics (direct-fed microbials) in poultry nutrition and their effects on nutrient utilization, growth and laying performance, and gut health: A systematic review. Animal, 10(10): 1863. https://doi.org/10.3390/ani10101863

Karimi-Torshizi MA, Moghaddam AR, Rahimi SH, Mojgani N (2010). Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response. Br. Poult. Sci., 51(2): 178-184. https://doi.org/10.1080/00071661003753756

Khan AZ, Kumbhar S, Liu Y, Hamid M, Pan C, Nido SA, Parveen F, Huang K (2018). Dietary supplementation of selenium-enriched probiotics enhances meat quality of broiler chickens (Gallus gallus domesticus) raised under high ambient temperature. Biol. Trace Elem. Res., 182: 328-338. https://doi.org/10.1007/s12011-017-1094-z

Khan S, Chousalkar KK (2021). Functional enrichment of gut microbiome by early supplementation of Bacillus based probiotic in cage free hens: A field study. Anim. Microbiome, 3(1): 1-18. https://doi.org/10.1186/s42523-021-00112-5

Khaziakhmetov F, Khabirov A, Avzalov R, Tsapalova G, Rebezov M, Tagirov K, Giniyatullinov S, Ishmuratov K, Mishukovskaya G, Gafarova F, Yessimbekov Z (2018). Valuable effect of using probiotics in poultry farming. Annu. Res. Rev. Biol., pp. 1-7. https://doi.org/10.9734/ARRB/2018/40070

Krysiak K, Konkol D, Korczy´nski, M (2021). Overview of the use of probiotics in poultry production. Animal, 11: 1620. https://doi.org/10.3390/ani11061620

Kumar P, Chatli M, Verma AK, Mehta N, Malav O, Kumar D, Sharma N (2017). Quality, functionality, and shelf life of fermented meat and meat products: A review. Crit. Rev. Food Sci. Nutr., 57: 2844-2856. https://doi.org/10.1080/10408398.2015.1074533

Laxminarayan R, Van Boeckel T, Teillant A (2015). The economic costs of withdrawing antimicrobial growth promoters from the livestock sector; OECD: Paris, France.

Lee K, Lee S, Lillehoj H, Li G, Jang S, Babu U, Park M, Kim D, Lillehoj E, Neumann A (2010). Effects of direct fed microbials on growth performance, gut morphometry, and immune characteristics in broiler chickens. Poult. Sci., (89): 203-216. https://doi.org/10.3382/ps.2009-00418

Liu X, Yan H, Le Lv QX, Yin C, Zhang K, Wang P, Hu J (2012). Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian-Australas. J. Anim. Sci., 25(5): 682. https://doi.org/10.5713/ajas.2011.11334

Malematja E, Manyelo TG, Sebola NA, Mabelebele M (2023). The role of insects in promoting the health and gut status of poultry. Comp. Clin. Pathol., pp. 1-13. https://doi.org/10.1007/s00580-023-03447-4

Malematja E, Mavasa NO, Manamela FC, Chitura T (2022). Gut health, morphometrics, and immunomodulation of poultry species in response to probiotic supplementation. Comp. Clin. Pathol., pp. 1-10.

Milner E, Stevens B, An M, Lam V, Ainsworth M, Dihle P, Segars K (2021). Utilizing probiotics for the prevention and treatment of gastrointestinal diseases. Front. Microbiol., 12: 689958. https://doi.org/10.3389/fmicb.2021.689958

Mohammed AA, Zaki RS, Negm EA, Mahmoud MA, Cheng HW (2021). Effects of dietary supplementation of a probiotic (Bacillus subtilis) on bone mass and meat quality of broiler chickens. Poult. Sci., 100(3): 100906. https://doi.org/10.1016/j.psj.2020.11.073

Olnood CG, Beski SS, Choct M, Iji PA (2015). Novel probiotics: Their effects on growth performance, gut development, microbial community and activity of broiler chickens. Anim. Nutr., 1(3): 184-191. https://doi.org/10.1016/j.aninu.2015.07.003

Park YH, Hamidon F, Rajangan C, Soh KP, Gan CY, Lim TS, Abdullah WN, Liong MT (2016). Application of probiotics for the production of safe and high-quality poultry meat. Korean J. Food Sci. Anim. Resour., 36(5): 567. https://doi.org/10.5851/kosfa.2016.36.5.567

Peralta-Sánchez JM, Martín-Platero AM, Ariza-Romero JJ, Rabelo-Ruiz M, Zurita-González MJ, Baños A, Rodríguez-Ruano SM, Maqueda M, Valdivia E, MartínezBueno M (2019). Egg production in poultry farming is improved by probiotic bacteria. Front. Microbiol., 10: 1042. https://doi.org/10.3389/fmicb.2019.01042

Poonam Jaiswal D, Srivastav AK (2021). A study on the assessment of the antimicrobial susceptibility pattern of microorganisms present in yogurt. Ann. Rom. Soc. Cell Biol., 25(6): 15171-15183. Retrieved from https://annalsofrscb.ro/index.php/journal/article/view/8566

Qorbanpour M, Fahim T, Javandel F, Nosrati M, Paz E, Seidavi A, Ragni M, Laudadio V, Tufarelli V (2018). Effect of dietary ginger (Zingiber officinale Roscoe) and multi-strain probiotic on growth and carcass traits, blood biochemistry, immune responses and intestinal microflora in broiler chickens. Animal, 8(7): 117. https://doi.org/10.3390/ani8070117

Ricke SC, Rothrock Jr MJ (2020). Gastrointestinal microbiomes of broilers and layer hens in alternative production systems. Poult. Sci., 99(2): 660-669. https://doi.org/10.1016/j.psj.2019.12.017

Ritzi MM, Abdelrahman W, Van-Heerden K, Mohnl M, Barrett NW, Dalloul RA (2016). Combination of probiotics and coccidiosis vaccine enhances protection against an Eimeria challenge. Vet. Res., 47(1): 1-8. https://doi.org/10.1186/s13567-016-0397-y

Rouhi M, Sohrabvandi S, Mortazavian A (2018). Probiotic fermented sausage: Viability of probiotic microorganisms and sensory characteristics. Crit. Rev. Food Sci. Nutr., 53: 331-348. https://doi.org/10.1080/10408398.2010.531407

Roy BC, Khatun A (2020). Effects of feeding double strain spores as a probiotic with or without antibiotic growth promoter on broiler performance. Asian J. Med. Biol. Res., 6(3): 400-407. https://doi.org/10.3329/ajmbr.v6i3.49787

Salim HM, Huque KS, Kamaruddin KM, Beg MDAH (2018). Global restriction of using antibiotic growth promoters and alternative strategies in poultry production. Sci. Prog., 101: 52–75. https://doi.org/10.3184/003685018X15173975498947

Salim HM, Kang HK, Akter N, Kim DW, Kim JH, Kim MJ, Na JC, Jong HB, Choi HC, Suh OS, Kim WK (2013). Supplementation of direct fed microbials as an alternative to antibiotic on growth performance, immune response, cecal microbial population, and ileal morphology of broiler chickens. Poult. Sci., 92(8): 2084-2090. https://doi.org/10.3382/ps.2012-02947

Sapsuha Y, Suprijatna E, Kismiati S, Sugiharto S (2021). Combination of probiotic and phythobiotic as an alternative for antibiotic growth promoter for broilers chickens. A review. Livest. Res. Rural. Dev., 33: 49. (Google Scholar).

Shi Z, Rothrock Jr MJ, Ricke SC (2019). Applications of microbiome analyses in alternative poultry broiler production systems. Front. Vet. Sci., 6: 157. https://doi.org/10.3389/fvets.2019.00157

Trabelsi I, Slima SB, Ktari N, Triki M, Abdehedi R, Abaza W, Moussa H, Abdeslam A, Salah RB (2019). Incorporation of probiotic strain in raw minced beef meat: Study of textural modification, lipid and protein oxidation and colour parameters during refrigerated storage. Meat Sci., 154: 29–36. https://doi.org/10.1016/j.meatsci.2019.04.005

World Health Organization (2018). Antimicrobial Resistance. Geneva: World Health Organization. https://apps.who.int/iris/handle/10665/326454

Yang X, Zhang B, Guo Y, Jiao P, Long F (2010). Effects of dietary lipids and Clostridium butyricum on fat deposition and meat quality of broiler chickens. J. Poult. Sci., 89(2): 254-260. https://doi.org/10.3382/ps.2009-00234

Zhang B, Yang X, Guo Y, Long F (2011). Effects of dietary lipids and Clostridium butyricum on the performance and the digestive tract of broiler chickens. Arch. Anim. Nutr., 65(4): 329-339. https://doi.org/10.1080/1745039X.2011.568274

Zhang L, Zhang L, Zhan XA, Zeng X, Zhou L, Cao G, Chen AG, Yang C (2016). Effects of dietary supplementation of probiotic, Clostridium butyricum, on growth performance, immune response, intestinal barrier function, and digestive enzyme activity in broiler chickens challenged with Escherichia coli K88. J. Anim. Sci. Biotechnol., 7(1): 1-9. https://doi.org/10.1186/s40104-016-0061-4

Zhang L, Zhang R, Jia H, Zhu Z, Li H, Ma Y (2021). Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens. Open Life Sci., 16(1): 311-322. https://doi.org/10.1515/biol-2021-0031