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Effect of probiotics in poultry for improving meat quality
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ScienceDirect Effect of probiotics in poultry for improving meat quality Teodora Popova The ban on the use of antibiotic growth promotors in many countries in order to satisfy the consumers’ demands for healthy and safe meat leads to increasing researchers’ interest in finding strategies to maintain chicken health and production. Probiotics which are live microbial compounds are considered a good alternative to antibiotics, as their use in poultry diets has been associated with positive effects on health and growth in birds. Changes in growth performance often affect various meat quality traits and in this context, more and more recent research show that using probiotics as dietary supplements exhibit potential as a natural way to improve poultry meat quality. The review discusses the changes in the physicochemical characteristics as well as fatty acids profile and oxidative stability in poultry meat as affected by various probiotics added to the diet of the birds. Address Institute of Animal Science, 2232 Kostinbrod, Bulgaria Corresponding author: Popova, Teodora ([email protected])
Current Opinion in Food Science 2017, 14:72–77 This review comes from a themed issue on Food microbiology Edited by Ursula Gonzales-Barron
http://dx.doi.org/10.1016/j.cofs.2017.01.008 2214-7993/ã 2017 Elsevier Ltd. All rights reserved.
Introduction: why probiotics? The production and consumption of poultry meat and in particular chicken meat, has been significantly increasing. This rapid growth is to a great extent associated to the demands of the consumers for a healthier diet and meat as its essential component. In addition to the high quality protein, chicken meat is rich in polyunsaturated fatty acids, especially n-3 PUFA that are beneficial for the human health [1]. As stated by Marangoni et al. [2], numerous epidemiological studies all over the world and in highly diverse population groups prove that poultry meat consumption within a balanced diet is associated with good health. Very often, to improve meat production through promoting growth rate, increasing feed conversion and preventing disease, poultry industry uses antibiotics [3,4]. Their extensive use, however, leads to imbalance of the intestinal microflora, appearance of resistant bacteria and also drug residues in the bird Current Opinion in Food Science 2017, 14:72–77
organism, and that was the reason for the antibiotics in livestock industry to be banned in many countries, including the European Union. Natural feed additives or ‘live probiotics’ are constantly gaining interest as one of the alternatives to antibiotics in the poultry industry [5]. The primary aim of the use of probiotics in poultry diet is to maintain and improve the performance of the birds [6,7,8], and also to prevent and control enteric pathogens [9,10,11,12]. In this context, increasing numbers of probiotic products are being developed and used in poultry nutrition [13].
What is a probiotic and possible ways to improve poultry meat quality The word ‘probiotic’ comes from the Greek words ‘pro’ and ‘biotic,’ meaning ‘for life’ [14] and was first used by Lilly & Stillwell in 1965 [15] as opposite to the word antibiotic, to designate unknown growth promoting substances produced by a ciliate protozoan that stimulated the growth of another ciliate. The joint Food and Agriculture Organization of the United Nations (FAO) and World Health Organization (WHO) Working Group defined probiotics as “live micro-organisms which when administered in adequate amounts confer a health benefit on the host” [16]. This definition is widely accepted and adopted by the International Scientific Association for Probiotics and Prebiotics [17]. As a whole probiotics consist of various types of microorganisms that improve gut microflora and affect both the local and systemic immune systems by secreting beneficial enzymes, organic acids, vitamins and nontoxic antibacterial substances upon ingestion. In the poultry the mode of action of probiotics is schematised on Figure 1. The microorganisms currently being used in probiotic preparations for poultry are varied and many (Table 1). Selection of probiotic strain should consider of attributes such as being of host origin, non-pathogenic, technologically suitable for industrial processes, acid-resistance and bile-resistance, adherence to the gut epithelial tissue, persistence in the gastrointestinal tract for short period. Also, probiotic should produce antimicrobial substances, modulate immune responses and influence the metabolic activities of the gut [19]. The research on the probiotic application in poultry industry emphasize more often on their influence on the growth performance of the birds and their carcass composition [20,21]. Changes in growth parameters, however, might be associated with alteration of meat quality characteristics, and thus on the one hand, the feeding strategies using probiotics exhibit potential as a natural way to improve poultry meat quality in vivo. On www.sciencedirect.com
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Figure 1
maintain normal intestinal microflora by competitive exclusion and antagonism
stimulate the immune system
Probiotics
alter metabolism by increasing digestive and decreasing bacterial enzyme activity and ammonia production
improve feed intake and digestion Current Opinion in Food Science
Mode of action of probiotics in poultry (adapted by Kabir [18]).
the other hand, some research report results on the effect of the application of probiotics post mortem, in the processed products of poultry meat, mainly concerning its safety [22].
Evaluation of the effect of dietary probiotics on the physicochemical characteristics of poultry meat Physicochemical properties of meat are important since they determine to a great extent the possibilities for its storage or further processing. They are interconnected and affect the sensory qualities of meat, therefore the influence of probiotics will be presented on the whole complex of these parameters. The pH of meat is a significant index of its quality and together with colour should be used in the evaluation of meat, especially for further purposes of storage [23]. It is closely related to other important characteristics such as
water holding capacity. Studies on the probiotic administration in poultry showed that pH might be influenced, but the results depend on the type of microorganisms and also on the specifics of the experimental design. Ivanovic et al. [24] studied the effect of two probiotics supplied in different amount to the diet of broiler chickens and found significant changes in the pH measured 24 hours post mortem in breast and thigh meat, which differed between the microorganisms used. Receiving 0.05% Streptococcus faecium cernelle 68 in the feed significantly decreased pH, while 0.01% of Bacillus cereus IP 5832 increased pH in both meat cuts. Zheng et al. [25] showed significantly higher pH in breast both 45 min and 24 hours post mortem in broilers receiving Enterococcus faecium in the diet which was accompanied by lower drip loss and cooking loss. In addition, there are studies examining the effect of probiotic on the quality characteristics of chicken meat while the latter has been subjected to storage. Mazaheri et al. [26] studied the influence of mushroom waste,
Table 1 Microorganisms used for probiotic preparations in poultry. Microorganisms Bacteria
Genus Lactobacillus
Species
Bifidobacterium Enterococcus Escherichia
thermophilus, acidophilus, brevis, bulgaricus, casei, fermentum, gallinarum, jensenii, plantarum, reuteri, rhamnosus, salivarius amilolique-facience, cereus, coagulans, licheniformis, megaterium, mesentericus, natto, polymixa, subtilis, animalis, bifidium, bifidus, thermophilus faecium coli
Fungi
Aspergillus
niger, oryzae
Yeasts
Saccharomyces
boulardii, cerevisiae, faecium, salivarius subsp. thermophilus
Bacillus
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considered rich source of bioactive compounds as well as four strain probiotic in broiler meat stored for 30 days. The authors reported significant decrease in the pH values of the meat throughout storage in the birds fed probiotic. Similarly, Abdullah et al. [27] observed significant decrease in the pH during storage of meat from broilers fed probiotic containing diet (Bacillus subtilis) when it was stored for 7 days. The colour of meat is important for the consumers’ perception of meat freshness and quality [28] and is determined by measuring its lightness (L*), redness (a*) and yellowness (b*) [29]. According to Jiang et al. [30] the redness is most favoured by consumers and lower b* values indicate less pale meat. In a study of Ha9c´ık et al. [31a] the use of probiotic in the water of broilers (Lactobacillus fermentum) significantly increased the redness in breast, while there was no effect on the yellowness and lightness in breast and thighs. In another study of the aforementioned authors [31b], however, the probiotic in combination with bee polen led to significant increase of redness and yellowness in thighs and also increased lightness in both breast and thigh cuts. Slightly reduced lightness in the meat of chickens following probiotic supplementation was observed in poultry receiving Bacillus subtilis [32] and Enterococcus faecium [25], while combination of Bacillus subtilis, Clostridium butyricum and Lactobacillus acidophilus [33] had stronger influence on this parameter. Improvement in colour characteristics in breast meat in terms of lightness and yellowness was found in a study of Abdurrahman et al. [34a]. The authors tested the effect of inulin and Lactobacillus at different levels in the chicken feed and found that the combination of both led to changes in b* and L* values; however, the results depended on the dose of administered pre-and probiotic. Probiotics containing Bacillus licheniformis in the poultry diet enhanced the meat colour, flavour and juiceness in fresh meat [35], while Bacillus subtillis showed negligible effect on the texture in cooked meat [36]. The research on the chemical composition of meat showed that the main traits affected by probiotic in the birds’ diet were protein and fat content. Bacillus licheniformis treatment increased significantly the protein content and respective content of essential and flavour amino acids, while on the other hand, the fat content was decreased [35]. Improved content of protein and reduced fat in birds fed probiotic containing Bacillus subtilis was found by Kra´l et al. [37]. Similar results were reported by Hossain et al. [38a], observing higher content of protein (25.9% vs. 23.4%), but lower fat in breast (0.56% vs. 0.24%) after dietary probiotic supplementation and by Abdurrahman et al. [34a,34b]. Considerably reduced fat content in the meat was found by Inatomi [39] when broilers received a combination of three probiotics Current Opinion in Food Science 2017, 14:72–77
(Bacillus mesentericus TO-A, Clostridium butyricum TO-A and Streptococcus faecalis T-110). In the breast of the birds consumed probiotics the fat content was 1.99% vs. 4.12% in the control group, while in thigh it was 7.10% for the control group and 5.66% in the birds receiving probiotics. Probiotics, especially lactic acid bacteria supplemented to broilers’ feed, appeared to considerably reduce the cholesterol content of meat [34a,40], thus having positive effect on its healthy value. The reduction of cholesterol could be achieved through its assimilation by bacterial growing cells or incorporation in the cellular surface of the probiotic microorganism, thus inhibiting the absorption of the cholesterol back in the body [41,42]. On the other hand, increased deconjugation of bile acids by bacterial hydrolases has been reported [43] increasing the cholesterol excretion of deconjugated bile salts and increasing cholesterol uptake and metabolism in the liver as compensatory response because it is known to constitute precursor for bile acids. In addition to the described hypolipidemic effect of probiotics, the short chain fatty acids they produce, especially propionate, could exert controlling effect on lowering hepatic lipogenesis and the inhibition of lipogenesis process [44] related to the decrease in meat fat content.
Influence of probiotics fed to birds on the lipid composition and oxidation of the meat Fatty acid composition is an important component of meat quality, associated with its dietetic value. Research on the influence of various probiotics on the fatty acid profile of meat is relatively scarce, but the overall results show positive effect of the probiotics, mainly related to reduction in saturated and increase of polyunsaturated fatty acids. Feeding broilers with Aspergillus awamori and Saccharomyces cerevisiae or combination of them led to significant decrease in the saturated C16:0 and C18:0, and increase in C18:1 as well as in the polyunsaturated C18:2, C18:3, C20:4 [45,46]. The same was observed when the diet of the birds contained Aspergillus awamori and Aspergillus niger in different amounts (0.01%, 0.05%, 0.1%) [47] as well as Aspergillus awamori in combination with selenium nanoparticles [48]. Hossain et al. [38a] also observed increase in the C18:3 in breast and C18:2 and C18:3 in the thighs after probiotic administration; however, in another experiment, Hossain et al. [38b] observed reduction in the n-6 PUFA in both breast and thigh. Further Ha9cı´k et al. [49] found slight increase of mono and polyunsaturated, while decrease in the saturated fatty acids in broilers fed probiotics alone or in combination with pollen. Lipid oxidation is one of the major causes for food quality deterioration. It is usually accompanied by development of off-odours and flavours, and also formation of substances considered cancerogenic. Usually the oxidation in foods, including meat, is measured by the content of www.sciencedirect.com
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thiobarbituric acid reactive substances (TBARS-test). Recent research showed either positive or lack of adverse effect of the probiotics on the lipid stability of chicken meat. Despite the increased content of PUFA and the higher total fat content reported by Saleh et al. [47], Aspergillus awamori and Aspergillus niger decreased significantly the content of TBARS in broiler breast in the birds receiving probiotic. The low lipid oxidation was accompanied with significantly increased content of muscle tocopherol in the supplemented groups. These results were further confirmed in other experiments [45,50] with birds fed Aspergillus awamori alone or combined with canola seed. When using probiotic based on Lactobacillus fermentum in the diet, Bobko et al. [51] observed reduced TBARS content in both breast (0.034 vs. 0.025 mg/kg meat) and thigh meat (0.043 vs. 0.033 mg/kg meat) on the first day of storage. Lower TBARS in meat, due to probiotics was reported in fresh meat (0.024 vs. 0.018 mg/kg meat) [33] and after 5, 7 and 14 days of storage [38a,38b]. Aristides et al. [32] reported considerably lower TBARS content in chicken meat after probiotic supplementation, however not significant, while Kim et al. [52] did not observe any difference in oxidative stability of chicken meat as affected by dietary probiotic supplementation. It could be seen that the majority of studies dedicated to the effect of the dietary probiotics on the lipid profile and oxidation in poultry meat report increased unsaturation of the fatty acids, but higher oxidative stability. Such results additionally confirm the fact that probiotics exhibit significant antioxidant activity observed in both in vitro and in vivo experiments [34b,53].
Conclusions The results of the recent studies on the application of probiotics in poultry showed that despite the various effects depending on the dose or microorganisms, they are mostly beneficial and hence probiotics might be used for improvement of pH, colour, water holding capacity, chemical composition, fatty acid profile and oxidative stability. Additionally, meta-analytical approach could be applied to assess precisely some of the contradictory effects of the probiotics reported in the studies. In future, research on the probiotics in poultry diets should continue in order to establish the most appropriate conditions at which the probiotics would exert their positive effect at the greatest extent in order to produce high quality and healthy poultry meat.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
N: Difference in the fatty Popova T, Ignatova M, Petkov E, Staniic acid composition and related nutritional indices of meat between two lines of slow-growing chickens slaughtered at different ages. Arch Anim Breed 2016, 59:319-327.
www.sciencedirect.com
2.
Marangoni F, Corsello G, Cricelli C, Ferrara N, Ghiselli A, Lucchin L, Poli A: Role of poultry meat in a balanced diet aimed at maintaining health and wellbeing: an Italian consensus document. Food Nutr Res 2015, 59:27606.
3.
Chattopadhyay MK: Use of antibiotics as feed additives: a burning question. Front Microbiol 2014, 5:334.
4.
Diarra MS, Malouin F: Antibiotics in Canadian poultry production and anticipated alternatives. Front Microbiol 2014, 5:282.
5.
Gupta AR, Das S: The benefits of probiotics in poultry production: an overview. Int J Livest Res 2013, 3:18-22.
6.
Mountzouris KC, Palamidi I, Tsirtsikos P, Mohnl M, Schatzmayr G, Fegeros K: Effect of dietary inclusion level of a multi-species probiotic on broiler performance and two biomarkers of their caecal ecology. Anim Prod Sci 2014, 55:484-493.
7.
Atela JA, Tuitoek J, Onjoro PA, Kibitok NK: Effects of probiotics feeding technology on weight gain of indigenous chicken in Kenya. IOSR—JAVS 2015, 8:33-36.
Lei X, Piao X, Ru Y, Zhang H, Pe´ron A, Zhang H: Effect of Bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian Australas J Anim Sci 2015, 28:239-246. The authors designed the study to assess the effect of the dietary supplementation of Bacillus amyloliquefaciens-based direct-fed microbial (DFM) on growth performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. The results indicate that Bacillus amyloliquefaciens-based DFM appeared to be promising alternative to the use of antibiotic growth promotors in broiler diets. Supplementation with 30 mg/kg and 60 mg/kg of Bacillus amyloliquefaciens-based DFM improved growth performance of broilers fed plant protein-based diets. This improvement was associated with the positive effect of nutrient utilization, intestinal morphology and cecal microflora
8.
9.
Ashraf S, Zaneb H, Yousaf MS, Ijaz A, Sohail MU, Muti S, Usman UU, Ijaz S, Rehman H: Effect of dietary supplementation of prebiotics and probiotics on intestinal microstructure in broilers reared under cyclic heat stress. J Anim Physiol Anim Nutr 2013, 97:68-73.
10. Argan˜araz-Martı´nez E, Babot JD, Apella MC, Perez Chaia A: Physiological and functional characteristics of Propionibacterium strains of the poultry microbiota and relevance for the development of probiotic products. Anaerobe 2013, 23:27-37. 11. Islam MR, Mostofa M, Islam S, Roy RR, Sorwar MG, Mondal KS: Role of max yeast culture probiotic in potentiating the growth performance of commercial broiler. Progress Agric 2013, 24:131-136. 12. Hsu YM, Yu B, Tseng CS, Chang CH, Chen DS, Su CH, Chen YS: Preventive activities of Scutellariae Radix, Gardeniae Fructus, and probiotics in Salmonella enterica serovar Typhimurium infection in chickens. Anim Feed Sci Technol 2016, 214:121-129. In this study, Scutellariae radix, Gardeniae fructus and probiotic-lactic acid bacteria were evaluated to determine their efficiency in preventing an infection from Salmonella enterica serovar Typhimurium in chickens. The results suggest that herbs and probiotic-lactic acid bacteria can clear the bacterial infection as well as suppress the inflammation response. Herbs and probiotic decreased Salmonella load in feces and intestinal tissues. Levels of IFN-g and IL-1b in intestinal tissues were reduced in all treated groups. Scutellariae radix and Gardeniae fructus with lactic acid bacteria suppressed the levels of IL-8 in serum and intestines. Herbs and lactic acid bacteria could be a natural way to replace antibiotics in feed additives. 13. Bajagai YS, Klieve AV, Dart PJ, Bryden WL: Probiotics in animal nutrition—Production, impact and regulation. Rome: FAO Animal Production and Health; 2016:. Paper No. 179. 14. Gibson GR, Fuller R: Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. J Nutr 2000, 130:391S-395S. 15. Lilly DM, Stillwell RH: Probiotics: growth-promoting factors produced by micro-organisms. Science 1965, 147:747-748. 16. Food and Agriculture organization of the United Nations/World Health Organization (FAO/WHO). Health and nutritional properties Current Opinion in Food Science 2017, 14:72–77
76 Food microbiology
of probiotics in food including powder milk with live lactic acid bacteria [Internet]. 2001: Report of a joint FAO/WHO expert consultation. 17. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S: Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014, 11:506-514. 18. Kabir LSM: The role of probiotics in the poultry industry. Int J Mol Sci 2009, 10:3531-3546. 19. Kossin B, Rakshit SK: Microbial and processing criteria for production of probiotics: a review. Food Technol Biotechnol 2006, 44:371-379. 20. Ignatova M, Sredkova V, Marasheva V: Effect of dietary inclusion of probiotic on chicken performance and some blood indices. Biotechnol Anim Husb 2009, 25:1079-1085. 21. Sarangi NR, Babu LK, Kumar A, Pradhan CR, Pati PK, Mishra JP: Effect of dietary supplementation of prebiotic, probitic, and symbiotic on growth performance and carcass characteristics of broiler chickens. Vet World 2016, 9:313-319. 22. Bomdespacho LQ, Cavallini DCU, Zavarizi ACM, Pinto RA, Rossi EA: Evaluation of the use of probiotic acid lactic bacteria in the development of chicken hamburger. Int Food Res J 2014, 21:965-972. 23. We?glarz A: Meat quality defined based on pH and colour depending on cattle category and slaughter season. Czech J Anim Sci 2010, 55:548-556. 24. Ivanovic S, Pisinov B, Maslic-Strizak D, Savic B, Stojanovic Z: Influence of probiotics on quality of chicken meat. Afr J Agric Res 2012, 7:2191-2196. 25. Zheng A, Luo J, Meng K, Li J, Zhang S, Liu G, Cai H, Bryden WL, Yao B: Proteome changes underpin improved meat quality and yield of chickens (Gallus gallus) fed the probiotic Enterococcus faecium. Genomics 2015, 15:1167. Supplementation of broiler chicken diets with probiotics appears to improve carcass characteristics and meat quality. However, the underlying molecular mechanism remains unclear. In this experiment 2D-DIGEbased proteomics was employed to investigate the proteome changes associated with improved carcass traits and meat quality of broilers fed the probiotic Enterococcus faecium. The probiotic significantly increased meat colour, water holding capacity and pH of breast while decreasing the abdominal fat content. These changes were related to the altered abundance of 22 proteins in the breast muscle after feeding probiotic. Of these, 17 proteins have central roles in regulating meat quality due to their biological interaction network. Altered cytoskeletal and chaperon protein expression also contribute to improved water holding capacity and colour of meat, which suggests that upregulation of chaperon proteins maintains cell integrity and prevents moisture loss by enhancing folding and recovery of the membrane and cytoskeletal proteins. The down-regulation of b-enolase and pyruvate kinase muscle isozymes suggests roles in increasing the pH of meat by decreasing the production of lactic acid. The validity of the proteomics results was further confirmed by qPCR. These results of the study reveals that improved meat quality of broilers fed probiotics is triggered by proteome alterations (especially the glycolytic proteins), and provides a new insight into the mechanism by which probiotics improve poultry production. 26. Mazaheri A, Shans Sargh M, Dastar B, Zerehdaran S: Effect of different levels of mushroom waste (Agaricus bisporus) with or without probiotic on growth performance: carcass characteristics, and breast meat quality in broiler chickens. Poult Sci J 2014, 2:125-138. 27. Abdulla NR, Zamri ANM, Sabow AB, Kareem KY, Nurhazirah S, Ling FH, Sazili AQ, Loh TC: Physico-chemical properties of breast muscle in broiler chickens fed probiotics, antibiotics or antibiotic-probiotic mix. J Appl Anim Res 2015 http://dx.doi.org/ 10.1080/09712119.2015.1124330. 28. Droval AA, Benassi VT, Rossa A, Prudencio SH, Paia˜o FG, Shimokomaki M: Consumer attitudes and preferences regarding pale: soft, and exudative broiler breast meat. J Appl Poult Res 2012, 21:502-507.
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29. Kadim IT, Mahgoub O: Structure and quality of camel meat. In Camel Meat and Meat Products. Edited by Kadim IT, Mahgoub O, Faye B, Farouk MM. CABI; 2013:124-153. 30. Jiang S, Jiang Z, Zhou G, Lin Y, Zheng C: Effects of dietary isoflavone supplementation on meat quality and oxidative stability during storage in lingnan yellow broilers. J Integr Agr 2014, 13(2):387-393. 31. (a). J, Bu9 Ha9 c´ık P, Trembecka´ L, Bobko M, Cubo n cko O, Tka´c9 ova´ J: Evaluation of meat quality after application of different feed additives in diet of broiler chickens. Potravinarstvo 2015, 9:174182; (b). Ha9 c´ık P, Trembecka´ L, Bobko M, Ka9 ca´niova´ M, Bu9 cko O, Tka´c9 ova´ J, Kunova´ S: Effect of different dietary supplements on selected quality indicators of chicken meat. Potravinarstvo 2015, 9:427-434. 32. Aristides LGA, Paia˜o FG, Murate LS, Oba A, Shimokomaki M: The effects of biotic additives on growth performance and meat qualities in broiler chickens. Int J Poult Sci 2012, 11:599-604. 33. Hossain MM, Begum M, Kim IH: Effect of Bacillus subtilis, Clostridium butyricum and Lactobacillus acidophilus endospores on growth performance, nutrient digestibility, meat quality, relative organ weight, microbial shedding and excreta noxious gas emission in broilers. Veterinarni Medicina 2015, 60:77-86. 34. (a). Abdurrahman ZH, Pramono YB, Suthama N: Meat characteristic of crossbred local chicken fed inulin of Dahlia Tuber and Lactobacillus sp. Med Pet 2016, 39:112-118; (b). Abdurrahman ZH, Pramono YB, Suthama N: Feeding effect of inulin derived from dahlia tuber combined with lactobacillus sp. on meat protein mass of crossbred kampong chicken. J Indonesian Trop Anim Agric 2016, 41:37-44. 35. Liu X, Yan H, Lv L, Xu Q, Yin C, Zhang K, Wang P, Hu J: Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian-Australas J Anim Sci 2012, 25:682-689. 36. Alfaig E, Angelovicova M, Kral M, Vietoris V, Zidek R: Effects of probiotic and thyme essential oil on the texture of cooked chicken breast meat. Acta Sci Pol Technol Aliment 2013, 12:379384. 37. Kra´l M, Angelovi9 cova´ M, Alfaig E, Walczycka M: Meat quality of broiler chickens fed diets with Bacillus subtilis and malic acid additives. Sci Pap Anim Sci Biotechnol 2013, 46:375-378. 38. (a). Hossain ME, Ko SY, Kim GM, Firman JD, Yang CJ: Evaluation of probiotic strains for development of fermented Alisma canaliculatum and their effects on broiler chickens. Poult Sci 2012, 91:3121-3131; (b). Hossain EM, Kim GM, Lee SK, Yang CJ: Growth performance: meat yield, oxidative stability and fatty acid composition of meat from broilers fed diet supplemented with a medicinal plant and probiotics. Asian-Australas J Anim Sci 2012, 25:11591168. 39. Inatomi T: Growth performance, gut mucosal immunity and carcass and intramuscular fat of broilers fed diet containing a combination of three probiotics. Sci Postprint 2015, 1:e00052. The study evaluates the effect of supplementing broiler diet with a combination of three probiotics on growth performance, gut mucosal immunity and carcass and intramuscular fat in broilers. The results indicated that probiotics containing B. mesentericus TO-A, C. butyricum TO-A and S. faecalis T-110 promote growth performance (average daily gain, feed conversion ratio, carcass yield), gut mucosal immunity (jejunum and ileum IgA concentration) and decrease abdominal and intramuscular fat in broiler chicken. It is therefore suggested that the use of probiotics would be advantageous to the poultry industry. 40. Astuti: The use of lactate acid bacterium, Streptococcus thermophilus from fish digestion organ to growth and colesterol level of chicken broiler strain Hubbart. Int J Dev Res 2015, 5:5695-5698. www.sciencedirect.com
Probiotics in poultry Popova 77
41. Aluwong T, Hassan F, Dzenda T, Kawu M, Ayo J: Effect of different levels of supplemental yeast on body weight, thyroid hormone metabolism and lipid profile of broiler chickens. J Vet Med Sci 2013, 75:291-298. 42. Salaj R, tofilova´ J, oltesova´ A, Hertelyova´ Z, Hijova´ E, Bertkova´ I, Strojny´ L, Kruzliak P, Bomba A: The effects of two lactobacillus plantarum strains on rat lipid metabolism receiving a high fat diet. Sci World J 2013, 2013 Article ID 135142, 7 p.. 43. Fajrih N, Suthama N, Yunianto VD: Body resistance and productive performance of crossbred local chicken fed inulin of dahlia tubers. Med Pet 2014, 37:108-144. 44. Weitkunat K, Schumann S, Petzke KJ, Blaut M, Loh G, Klaus S: Effects of dietary inulin on bacterial growth, short-chain fatty acid production and hepatic lipid metabolism in gnotobiotic mice. J Nut Biochem 2015, 26:929-937. 45. Saleh AA, Eid YZ, Ebeid TA, Ohtsuka A, Hioki K, Yamamoto M, Hayashi K: The modification of the muscle fatty acid profile by dietary supplementation with Aspergillus awamori in broiler chickens. Br J Nutr 2012, 108:1596-1602. 46. Saleh AA, Hayashi K, Ohtsuka A: Synergistic effect of feeding Aspergillus awamori and Saccharomyces cerevisiae on growth performance in broiler chickens; promotion of protein metabolism and modification of fatty acid profile in the muscle. J Poult Sci 2013, 50:242-250. 47. Saleh AA, Eid YZ, Ebeid YZ, Kamizono T, Ohtsuka A, Hayashi K: Effects of feeding Aspergillus awamori and Aspergillus niger on growth performance and meat quality in broiler chickens. J Poult Sci 2011, 48:201-206. 48. Saleh AA: Effect of feeding mixture of Aspergillus probiotic and selenium nano-particles on growth, nutrient digestibilities,
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selected blood parameters and muscle fatty acid profile in broiler chickens. Anim Sci Pap Rep 2014, 32:65-79. c´ık P, Elimam I, Garlı´k J, Bobko M, Tka´c9 ova´ J, Trembecka´ L, 49. Ha9 Ka9 ca´niova´ M: Fatty acid content in broilers Ross 308 meat muscles after using bee pollen and probiotic as supplementary diet into their mixture. Microbiol Biotech Food Sci 2014, 4:67-69. 50. Saleh AA, Hayashi K, Ijiri D, Ohtsuka A: Effect of feeding Aspergillus awamori and canola seed on the growth performance and muscle fatty acid profile in broiler chicken. Anim Sci J 2014, 86:305-311. 51. Bobko M, Ha9 cı´k P, Bobkova´ A, Pavelkova´ A, Tka´c9 ova´ J, Trembecka´ L: Lipid oxidation in chicken meat after application of bee pollen extract, propolis extract and probiotic in their diets. Potravinarstvo 2015, 9:342-346. In the experiment, the effect of the addition of bee pollen, propolis extract and probiotic in a feed mixture for chicken broilers on oxidative stability of breast and thigh muscles during chilled storage was investigated. Results achieved showed that the addition of propolis extract in feed mixture for broiler chickens had positive impact on the reduction of oxidative processes in the breast and thigh muscles during chilling storage, but with the addition of bee pollen extract and probiotic, significant effect on the oxidation of fat in the breast and thigh muscles of meat broiler chickens has been recorded. 52. Kim HW, Yan FF, Hu JY, Cheng HW, Kim YH: Effects of probiotics feeding on meat quality of chicken breast during postmortem storage. Poult Sci 2016, 95:1457-1464. 53. Pieniz S, Andreazza R, Anghinoni T, Camargo F, Brandelli A: Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 2014, 37:251-256.
Current Opinion in Food Science 2017, 14:72–77
ScienceDirect Effect of probiotics in poultry for improving meat quality Teodora Popova The ban on the use of antibiotic growth promotors in many countries in order to satisfy the consumers’ demands for healthy and safe meat leads to increasing researchers’ interest in finding strategies to maintain chicken health and production. Probiotics which are live microbial compounds are considered a good alternative to antibiotics, as their use in poultry diets has been associated with positive effects on health and growth in birds. Changes in growth performance often affect various meat quality traits and in this context, more and more recent research show that using probiotics as dietary supplements exhibit potential as a natural way to improve poultry meat quality. The review discusses the changes in the physicochemical characteristics as well as fatty acids profile and oxidative stability in poultry meat as affected by various probiotics added to the diet of the birds. Address Institute of Animal Science, 2232 Kostinbrod, Bulgaria Corresponding author: Popova, Teodora ([email protected])
Current Opinion in Food Science 2017, 14:72–77 This review comes from a themed issue on Food microbiology Edited by Ursula Gonzales-Barron
http://dx.doi.org/10.1016/j.cofs.2017.01.008 2214-7993/ã 2017 Elsevier Ltd. All rights reserved.
Introduction: why probiotics? The production and consumption of poultry meat and in particular chicken meat, has been significantly increasing. This rapid growth is to a great extent associated to the demands of the consumers for a healthier diet and meat as its essential component. In addition to the high quality protein, chicken meat is rich in polyunsaturated fatty acids, especially n-3 PUFA that are beneficial for the human health [1]. As stated by Marangoni et al. [2], numerous epidemiological studies all over the world and in highly diverse population groups prove that poultry meat consumption within a balanced diet is associated with good health. Very often, to improve meat production through promoting growth rate, increasing feed conversion and preventing disease, poultry industry uses antibiotics [3,4]. Their extensive use, however, leads to imbalance of the intestinal microflora, appearance of resistant bacteria and also drug residues in the bird Current Opinion in Food Science 2017, 14:72–77
organism, and that was the reason for the antibiotics in livestock industry to be banned in many countries, including the European Union. Natural feed additives or ‘live probiotics’ are constantly gaining interest as one of the alternatives to antibiotics in the poultry industry [5]. The primary aim of the use of probiotics in poultry diet is to maintain and improve the performance of the birds [6,7,8], and also to prevent and control enteric pathogens [9,10,11,12]. In this context, increasing numbers of probiotic products are being developed and used in poultry nutrition [13].
What is a probiotic and possible ways to improve poultry meat quality The word ‘probiotic’ comes from the Greek words ‘pro’ and ‘biotic,’ meaning ‘for life’ [14] and was first used by Lilly & Stillwell in 1965 [15] as opposite to the word antibiotic, to designate unknown growth promoting substances produced by a ciliate protozoan that stimulated the growth of another ciliate. The joint Food and Agriculture Organization of the United Nations (FAO) and World Health Organization (WHO) Working Group defined probiotics as “live micro-organisms which when administered in adequate amounts confer a health benefit on the host” [16]. This definition is widely accepted and adopted by the International Scientific Association for Probiotics and Prebiotics [17]. As a whole probiotics consist of various types of microorganisms that improve gut microflora and affect both the local and systemic immune systems by secreting beneficial enzymes, organic acids, vitamins and nontoxic antibacterial substances upon ingestion. In the poultry the mode of action of probiotics is schematised on Figure 1. The microorganisms currently being used in probiotic preparations for poultry are varied and many (Table 1). Selection of probiotic strain should consider of attributes such as being of host origin, non-pathogenic, technologically suitable for industrial processes, acid-resistance and bile-resistance, adherence to the gut epithelial tissue, persistence in the gastrointestinal tract for short period. Also, probiotic should produce antimicrobial substances, modulate immune responses and influence the metabolic activities of the gut [19]. The research on the probiotic application in poultry industry emphasize more often on their influence on the growth performance of the birds and their carcass composition [20,21]. Changes in growth parameters, however, might be associated with alteration of meat quality characteristics, and thus on the one hand, the feeding strategies using probiotics exhibit potential as a natural way to improve poultry meat quality in vivo. On www.sciencedirect.com
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Figure 1
maintain normal intestinal microflora by competitive exclusion and antagonism
stimulate the immune system
Probiotics
alter metabolism by increasing digestive and decreasing bacterial enzyme activity and ammonia production
improve feed intake and digestion Current Opinion in Food Science
Mode of action of probiotics in poultry (adapted by Kabir [18]).
the other hand, some research report results on the effect of the application of probiotics post mortem, in the processed products of poultry meat, mainly concerning its safety [22].
Evaluation of the effect of dietary probiotics on the physicochemical characteristics of poultry meat Physicochemical properties of meat are important since they determine to a great extent the possibilities for its storage or further processing. They are interconnected and affect the sensory qualities of meat, therefore the influence of probiotics will be presented on the whole complex of these parameters. The pH of meat is a significant index of its quality and together with colour should be used in the evaluation of meat, especially for further purposes of storage [23]. It is closely related to other important characteristics such as
water holding capacity. Studies on the probiotic administration in poultry showed that pH might be influenced, but the results depend on the type of microorganisms and also on the specifics of the experimental design. Ivanovic et al. [24] studied the effect of two probiotics supplied in different amount to the diet of broiler chickens and found significant changes in the pH measured 24 hours post mortem in breast and thigh meat, which differed between the microorganisms used. Receiving 0.05% Streptococcus faecium cernelle 68 in the feed significantly decreased pH, while 0.01% of Bacillus cereus IP 5832 increased pH in both meat cuts. Zheng et al. [25] showed significantly higher pH in breast both 45 min and 24 hours post mortem in broilers receiving Enterococcus faecium in the diet which was accompanied by lower drip loss and cooking loss. In addition, there are studies examining the effect of probiotic on the quality characteristics of chicken meat while the latter has been subjected to storage. Mazaheri et al. [26] studied the influence of mushroom waste,
Table 1 Microorganisms used for probiotic preparations in poultry. Microorganisms Bacteria
Genus Lactobacillus
Species
Bifidobacterium Enterococcus Escherichia
thermophilus, acidophilus, brevis, bulgaricus, casei, fermentum, gallinarum, jensenii, plantarum, reuteri, rhamnosus, salivarius amilolique-facience, cereus, coagulans, licheniformis, megaterium, mesentericus, natto, polymixa, subtilis, animalis, bifidium, bifidus, thermophilus faecium coli
Fungi
Aspergillus
niger, oryzae
Yeasts
Saccharomyces
boulardii, cerevisiae, faecium, salivarius subsp. thermophilus
Bacillus
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considered rich source of bioactive compounds as well as four strain probiotic in broiler meat stored for 30 days. The authors reported significant decrease in the pH values of the meat throughout storage in the birds fed probiotic. Similarly, Abdullah et al. [27] observed significant decrease in the pH during storage of meat from broilers fed probiotic containing diet (Bacillus subtilis) when it was stored for 7 days. The colour of meat is important for the consumers’ perception of meat freshness and quality [28] and is determined by measuring its lightness (L*), redness (a*) and yellowness (b*) [29]. According to Jiang et al. [30] the redness is most favoured by consumers and lower b* values indicate less pale meat. In a study of Ha9c´ık et al. [31a] the use of probiotic in the water of broilers (Lactobacillus fermentum) significantly increased the redness in breast, while there was no effect on the yellowness and lightness in breast and thighs. In another study of the aforementioned authors [31b], however, the probiotic in combination with bee polen led to significant increase of redness and yellowness in thighs and also increased lightness in both breast and thigh cuts. Slightly reduced lightness in the meat of chickens following probiotic supplementation was observed in poultry receiving Bacillus subtilis [32] and Enterococcus faecium [25], while combination of Bacillus subtilis, Clostridium butyricum and Lactobacillus acidophilus [33] had stronger influence on this parameter. Improvement in colour characteristics in breast meat in terms of lightness and yellowness was found in a study of Abdurrahman et al. [34a]. The authors tested the effect of inulin and Lactobacillus at different levels in the chicken feed and found that the combination of both led to changes in b* and L* values; however, the results depended on the dose of administered pre-and probiotic. Probiotics containing Bacillus licheniformis in the poultry diet enhanced the meat colour, flavour and juiceness in fresh meat [35], while Bacillus subtillis showed negligible effect on the texture in cooked meat [36]. The research on the chemical composition of meat showed that the main traits affected by probiotic in the birds’ diet were protein and fat content. Bacillus licheniformis treatment increased significantly the protein content and respective content of essential and flavour amino acids, while on the other hand, the fat content was decreased [35]. Improved content of protein and reduced fat in birds fed probiotic containing Bacillus subtilis was found by Kra´l et al. [37]. Similar results were reported by Hossain et al. [38a], observing higher content of protein (25.9% vs. 23.4%), but lower fat in breast (0.56% vs. 0.24%) after dietary probiotic supplementation and by Abdurrahman et al. [34a,34b]. Considerably reduced fat content in the meat was found by Inatomi [39] when broilers received a combination of three probiotics Current Opinion in Food Science 2017, 14:72–77
(Bacillus mesentericus TO-A, Clostridium butyricum TO-A and Streptococcus faecalis T-110). In the breast of the birds consumed probiotics the fat content was 1.99% vs. 4.12% in the control group, while in thigh it was 7.10% for the control group and 5.66% in the birds receiving probiotics. Probiotics, especially lactic acid bacteria supplemented to broilers’ feed, appeared to considerably reduce the cholesterol content of meat [34a,40], thus having positive effect on its healthy value. The reduction of cholesterol could be achieved through its assimilation by bacterial growing cells or incorporation in the cellular surface of the probiotic microorganism, thus inhibiting the absorption of the cholesterol back in the body [41,42]. On the other hand, increased deconjugation of bile acids by bacterial hydrolases has been reported [43] increasing the cholesterol excretion of deconjugated bile salts and increasing cholesterol uptake and metabolism in the liver as compensatory response because it is known to constitute precursor for bile acids. In addition to the described hypolipidemic effect of probiotics, the short chain fatty acids they produce, especially propionate, could exert controlling effect on lowering hepatic lipogenesis and the inhibition of lipogenesis process [44] related to the decrease in meat fat content.
Influence of probiotics fed to birds on the lipid composition and oxidation of the meat Fatty acid composition is an important component of meat quality, associated with its dietetic value. Research on the influence of various probiotics on the fatty acid profile of meat is relatively scarce, but the overall results show positive effect of the probiotics, mainly related to reduction in saturated and increase of polyunsaturated fatty acids. Feeding broilers with Aspergillus awamori and Saccharomyces cerevisiae or combination of them led to significant decrease in the saturated C16:0 and C18:0, and increase in C18:1 as well as in the polyunsaturated C18:2, C18:3, C20:4 [45,46]. The same was observed when the diet of the birds contained Aspergillus awamori and Aspergillus niger in different amounts (0.01%, 0.05%, 0.1%) [47] as well as Aspergillus awamori in combination with selenium nanoparticles [48]. Hossain et al. [38a] also observed increase in the C18:3 in breast and C18:2 and C18:3 in the thighs after probiotic administration; however, in another experiment, Hossain et al. [38b] observed reduction in the n-6 PUFA in both breast and thigh. Further Ha9cı´k et al. [49] found slight increase of mono and polyunsaturated, while decrease in the saturated fatty acids in broilers fed probiotics alone or in combination with pollen. Lipid oxidation is one of the major causes for food quality deterioration. It is usually accompanied by development of off-odours and flavours, and also formation of substances considered cancerogenic. Usually the oxidation in foods, including meat, is measured by the content of www.sciencedirect.com
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thiobarbituric acid reactive substances (TBARS-test). Recent research showed either positive or lack of adverse effect of the probiotics on the lipid stability of chicken meat. Despite the increased content of PUFA and the higher total fat content reported by Saleh et al. [47], Aspergillus awamori and Aspergillus niger decreased significantly the content of TBARS in broiler breast in the birds receiving probiotic. The low lipid oxidation was accompanied with significantly increased content of muscle tocopherol in the supplemented groups. These results were further confirmed in other experiments [45,50] with birds fed Aspergillus awamori alone or combined with canola seed. When using probiotic based on Lactobacillus fermentum in the diet, Bobko et al. [51] observed reduced TBARS content in both breast (0.034 vs. 0.025 mg/kg meat) and thigh meat (0.043 vs. 0.033 mg/kg meat) on the first day of storage. Lower TBARS in meat, due to probiotics was reported in fresh meat (0.024 vs. 0.018 mg/kg meat) [33] and after 5, 7 and 14 days of storage [38a,38b]. Aristides et al. [32] reported considerably lower TBARS content in chicken meat after probiotic supplementation, however not significant, while Kim et al. [52] did not observe any difference in oxidative stability of chicken meat as affected by dietary probiotic supplementation. It could be seen that the majority of studies dedicated to the effect of the dietary probiotics on the lipid profile and oxidation in poultry meat report increased unsaturation of the fatty acids, but higher oxidative stability. Such results additionally confirm the fact that probiotics exhibit significant antioxidant activity observed in both in vitro and in vivo experiments [34b,53].
Conclusions The results of the recent studies on the application of probiotics in poultry showed that despite the various effects depending on the dose or microorganisms, they are mostly beneficial and hence probiotics might be used for improvement of pH, colour, water holding capacity, chemical composition, fatty acid profile and oxidative stability. Additionally, meta-analytical approach could be applied to assess precisely some of the contradictory effects of the probiotics reported in the studies. In future, research on the probiotics in poultry diets should continue in order to establish the most appropriate conditions at which the probiotics would exert their positive effect at the greatest extent in order to produce high quality and healthy poultry meat.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
N: Difference in the fatty Popova T, Ignatova M, Petkov E, Staniic acid composition and related nutritional indices of meat between two lines of slow-growing chickens slaughtered at different ages. Arch Anim Breed 2016, 59:319-327.
www.sciencedirect.com
2.
Marangoni F, Corsello G, Cricelli C, Ferrara N, Ghiselli A, Lucchin L, Poli A: Role of poultry meat in a balanced diet aimed at maintaining health and wellbeing: an Italian consensus document. Food Nutr Res 2015, 59:27606.
3.
Chattopadhyay MK: Use of antibiotics as feed additives: a burning question. Front Microbiol 2014, 5:334.
4.
Diarra MS, Malouin F: Antibiotics in Canadian poultry production and anticipated alternatives. Front Microbiol 2014, 5:282.
5.
Gupta AR, Das S: The benefits of probiotics in poultry production: an overview. Int J Livest Res 2013, 3:18-22.
6.
Mountzouris KC, Palamidi I, Tsirtsikos P, Mohnl M, Schatzmayr G, Fegeros K: Effect of dietary inclusion level of a multi-species probiotic on broiler performance and two biomarkers of their caecal ecology. Anim Prod Sci 2014, 55:484-493.
7.
Atela JA, Tuitoek J, Onjoro PA, Kibitok NK: Effects of probiotics feeding technology on weight gain of indigenous chicken in Kenya. IOSR—JAVS 2015, 8:33-36.
Lei X, Piao X, Ru Y, Zhang H, Pe´ron A, Zhang H: Effect of Bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian Australas J Anim Sci 2015, 28:239-246. The authors designed the study to assess the effect of the dietary supplementation of Bacillus amyloliquefaciens-based direct-fed microbial (DFM) on growth performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. The results indicate that Bacillus amyloliquefaciens-based DFM appeared to be promising alternative to the use of antibiotic growth promotors in broiler diets. Supplementation with 30 mg/kg and 60 mg/kg of Bacillus amyloliquefaciens-based DFM improved growth performance of broilers fed plant protein-based diets. This improvement was associated with the positive effect of nutrient utilization, intestinal morphology and cecal microflora
8.
9.
Ashraf S, Zaneb H, Yousaf MS, Ijaz A, Sohail MU, Muti S, Usman UU, Ijaz S, Rehman H: Effect of dietary supplementation of prebiotics and probiotics on intestinal microstructure in broilers reared under cyclic heat stress. J Anim Physiol Anim Nutr 2013, 97:68-73.
10. Argan˜araz-Martı´nez E, Babot JD, Apella MC, Perez Chaia A: Physiological and functional characteristics of Propionibacterium strains of the poultry microbiota and relevance for the development of probiotic products. Anaerobe 2013, 23:27-37. 11. Islam MR, Mostofa M, Islam S, Roy RR, Sorwar MG, Mondal KS: Role of max yeast culture probiotic in potentiating the growth performance of commercial broiler. Progress Agric 2013, 24:131-136. 12. Hsu YM, Yu B, Tseng CS, Chang CH, Chen DS, Su CH, Chen YS: Preventive activities of Scutellariae Radix, Gardeniae Fructus, and probiotics in Salmonella enterica serovar Typhimurium infection in chickens. Anim Feed Sci Technol 2016, 214:121-129. In this study, Scutellariae radix, Gardeniae fructus and probiotic-lactic acid bacteria were evaluated to determine their efficiency in preventing an infection from Salmonella enterica serovar Typhimurium in chickens. The results suggest that herbs and probiotic-lactic acid bacteria can clear the bacterial infection as well as suppress the inflammation response. Herbs and probiotic decreased Salmonella load in feces and intestinal tissues. Levels of IFN-g and IL-1b in intestinal tissues were reduced in all treated groups. Scutellariae radix and Gardeniae fructus with lactic acid bacteria suppressed the levels of IL-8 in serum and intestines. Herbs and lactic acid bacteria could be a natural way to replace antibiotics in feed additives. 13. Bajagai YS, Klieve AV, Dart PJ, Bryden WL: Probiotics in animal nutrition—Production, impact and regulation. Rome: FAO Animal Production and Health; 2016:. Paper No. 179. 14. Gibson GR, Fuller R: Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. J Nutr 2000, 130:391S-395S. 15. Lilly DM, Stillwell RH: Probiotics: growth-promoting factors produced by micro-organisms. Science 1965, 147:747-748. 16. Food and Agriculture organization of the United Nations/World Health Organization (FAO/WHO). Health and nutritional properties Current Opinion in Food Science 2017, 14:72–77
76 Food microbiology
of probiotics in food including powder milk with live lactic acid bacteria [Internet]. 2001: Report of a joint FAO/WHO expert consultation. 17. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S: Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014, 11:506-514. 18. Kabir LSM: The role of probiotics in the poultry industry. Int J Mol Sci 2009, 10:3531-3546. 19. Kossin B, Rakshit SK: Microbial and processing criteria for production of probiotics: a review. Food Technol Biotechnol 2006, 44:371-379. 20. Ignatova M, Sredkova V, Marasheva V: Effect of dietary inclusion of probiotic on chicken performance and some blood indices. Biotechnol Anim Husb 2009, 25:1079-1085. 21. Sarangi NR, Babu LK, Kumar A, Pradhan CR, Pati PK, Mishra JP: Effect of dietary supplementation of prebiotic, probitic, and symbiotic on growth performance and carcass characteristics of broiler chickens. Vet World 2016, 9:313-319. 22. Bomdespacho LQ, Cavallini DCU, Zavarizi ACM, Pinto RA, Rossi EA: Evaluation of the use of probiotic acid lactic bacteria in the development of chicken hamburger. Int Food Res J 2014, 21:965-972. 23. We?glarz A: Meat quality defined based on pH and colour depending on cattle category and slaughter season. Czech J Anim Sci 2010, 55:548-556. 24. Ivanovic S, Pisinov B, Maslic-Strizak D, Savic B, Stojanovic Z: Influence of probiotics on quality of chicken meat. Afr J Agric Res 2012, 7:2191-2196. 25. Zheng A, Luo J, Meng K, Li J, Zhang S, Liu G, Cai H, Bryden WL, Yao B: Proteome changes underpin improved meat quality and yield of chickens (Gallus gallus) fed the probiotic Enterococcus faecium. Genomics 2015, 15:1167. Supplementation of broiler chicken diets with probiotics appears to improve carcass characteristics and meat quality. However, the underlying molecular mechanism remains unclear. In this experiment 2D-DIGEbased proteomics was employed to investigate the proteome changes associated with improved carcass traits and meat quality of broilers fed the probiotic Enterococcus faecium. The probiotic significantly increased meat colour, water holding capacity and pH of breast while decreasing the abdominal fat content. These changes were related to the altered abundance of 22 proteins in the breast muscle after feeding probiotic. Of these, 17 proteins have central roles in regulating meat quality due to their biological interaction network. Altered cytoskeletal and chaperon protein expression also contribute to improved water holding capacity and colour of meat, which suggests that upregulation of chaperon proteins maintains cell integrity and prevents moisture loss by enhancing folding and recovery of the membrane and cytoskeletal proteins. The down-regulation of b-enolase and pyruvate kinase muscle isozymes suggests roles in increasing the pH of meat by decreasing the production of lactic acid. The validity of the proteomics results was further confirmed by qPCR. These results of the study reveals that improved meat quality of broilers fed probiotics is triggered by proteome alterations (especially the glycolytic proteins), and provides a new insight into the mechanism by which probiotics improve poultry production. 26. Mazaheri A, Shans Sargh M, Dastar B, Zerehdaran S: Effect of different levels of mushroom waste (Agaricus bisporus) with or without probiotic on growth performance: carcass characteristics, and breast meat quality in broiler chickens. Poult Sci J 2014, 2:125-138. 27. Abdulla NR, Zamri ANM, Sabow AB, Kareem KY, Nurhazirah S, Ling FH, Sazili AQ, Loh TC: Physico-chemical properties of breast muscle in broiler chickens fed probiotics, antibiotics or antibiotic-probiotic mix. J Appl Anim Res 2015 http://dx.doi.org/ 10.1080/09712119.2015.1124330. 28. Droval AA, Benassi VT, Rossa A, Prudencio SH, Paia˜o FG, Shimokomaki M: Consumer attitudes and preferences regarding pale: soft, and exudative broiler breast meat. J Appl Poult Res 2012, 21:502-507.
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29. Kadim IT, Mahgoub O: Structure and quality of camel meat. In Camel Meat and Meat Products. Edited by Kadim IT, Mahgoub O, Faye B, Farouk MM. CABI; 2013:124-153. 30. Jiang S, Jiang Z, Zhou G, Lin Y, Zheng C: Effects of dietary isoflavone supplementation on meat quality and oxidative stability during storage in lingnan yellow broilers. J Integr Agr 2014, 13(2):387-393. 31. (a). J, Bu9 Ha9 c´ık P, Trembecka´ L, Bobko M, Cubo n cko O, Tka´c9 ova´ J: Evaluation of meat quality after application of different feed additives in diet of broiler chickens. Potravinarstvo 2015, 9:174182; (b). Ha9 c´ık P, Trembecka´ L, Bobko M, Ka9 ca´niova´ M, Bu9 cko O, Tka´c9 ova´ J, Kunova´ S: Effect of different dietary supplements on selected quality indicators of chicken meat. Potravinarstvo 2015, 9:427-434. 32. Aristides LGA, Paia˜o FG, Murate LS, Oba A, Shimokomaki M: The effects of biotic additives on growth performance and meat qualities in broiler chickens. Int J Poult Sci 2012, 11:599-604. 33. Hossain MM, Begum M, Kim IH: Effect of Bacillus subtilis, Clostridium butyricum and Lactobacillus acidophilus endospores on growth performance, nutrient digestibility, meat quality, relative organ weight, microbial shedding and excreta noxious gas emission in broilers. Veterinarni Medicina 2015, 60:77-86. 34. (a). Abdurrahman ZH, Pramono YB, Suthama N: Meat characteristic of crossbred local chicken fed inulin of Dahlia Tuber and Lactobacillus sp. Med Pet 2016, 39:112-118; (b). Abdurrahman ZH, Pramono YB, Suthama N: Feeding effect of inulin derived from dahlia tuber combined with lactobacillus sp. on meat protein mass of crossbred kampong chicken. J Indonesian Trop Anim Agric 2016, 41:37-44. 35. Liu X, Yan H, Lv L, Xu Q, Yin C, Zhang K, Wang P, Hu J: Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian-Australas J Anim Sci 2012, 25:682-689. 36. Alfaig E, Angelovicova M, Kral M, Vietoris V, Zidek R: Effects of probiotic and thyme essential oil on the texture of cooked chicken breast meat. Acta Sci Pol Technol Aliment 2013, 12:379384. 37. Kra´l M, Angelovi9 cova´ M, Alfaig E, Walczycka M: Meat quality of broiler chickens fed diets with Bacillus subtilis and malic acid additives. Sci Pap Anim Sci Biotechnol 2013, 46:375-378. 38. (a). Hossain ME, Ko SY, Kim GM, Firman JD, Yang CJ: Evaluation of probiotic strains for development of fermented Alisma canaliculatum and their effects on broiler chickens. Poult Sci 2012, 91:3121-3131; (b). Hossain EM, Kim GM, Lee SK, Yang CJ: Growth performance: meat yield, oxidative stability and fatty acid composition of meat from broilers fed diet supplemented with a medicinal plant and probiotics. Asian-Australas J Anim Sci 2012, 25:11591168. 39. Inatomi T: Growth performance, gut mucosal immunity and carcass and intramuscular fat of broilers fed diet containing a combination of three probiotics. Sci Postprint 2015, 1:e00052. The study evaluates the effect of supplementing broiler diet with a combination of three probiotics on growth performance, gut mucosal immunity and carcass and intramuscular fat in broilers. The results indicated that probiotics containing B. mesentericus TO-A, C. butyricum TO-A and S. faecalis T-110 promote growth performance (average daily gain, feed conversion ratio, carcass yield), gut mucosal immunity (jejunum and ileum IgA concentration) and decrease abdominal and intramuscular fat in broiler chicken. It is therefore suggested that the use of probiotics would be advantageous to the poultry industry. 40. Astuti: The use of lactate acid bacterium, Streptococcus thermophilus from fish digestion organ to growth and colesterol level of chicken broiler strain Hubbart. Int J Dev Res 2015, 5:5695-5698. www.sciencedirect.com
Probiotics in poultry Popova 77
41. Aluwong T, Hassan F, Dzenda T, Kawu M, Ayo J: Effect of different levels of supplemental yeast on body weight, thyroid hormone metabolism and lipid profile of broiler chickens. J Vet Med Sci 2013, 75:291-298. 42. Salaj R, tofilova´ J, oltesova´ A, Hertelyova´ Z, Hijova´ E, Bertkova´ I, Strojny´ L, Kruzliak P, Bomba A: The effects of two lactobacillus plantarum strains on rat lipid metabolism receiving a high fat diet. Sci World J 2013, 2013 Article ID 135142, 7 p.. 43. Fajrih N, Suthama N, Yunianto VD: Body resistance and productive performance of crossbred local chicken fed inulin of dahlia tubers. Med Pet 2014, 37:108-144. 44. Weitkunat K, Schumann S, Petzke KJ, Blaut M, Loh G, Klaus S: Effects of dietary inulin on bacterial growth, short-chain fatty acid production and hepatic lipid metabolism in gnotobiotic mice. J Nut Biochem 2015, 26:929-937. 45. Saleh AA, Eid YZ, Ebeid TA, Ohtsuka A, Hioki K, Yamamoto M, Hayashi K: The modification of the muscle fatty acid profile by dietary supplementation with Aspergillus awamori in broiler chickens. Br J Nutr 2012, 108:1596-1602. 46. Saleh AA, Hayashi K, Ohtsuka A: Synergistic effect of feeding Aspergillus awamori and Saccharomyces cerevisiae on growth performance in broiler chickens; promotion of protein metabolism and modification of fatty acid profile in the muscle. J Poult Sci 2013, 50:242-250. 47. Saleh AA, Eid YZ, Ebeid YZ, Kamizono T, Ohtsuka A, Hayashi K: Effects of feeding Aspergillus awamori and Aspergillus niger on growth performance and meat quality in broiler chickens. J Poult Sci 2011, 48:201-206. 48. Saleh AA: Effect of feeding mixture of Aspergillus probiotic and selenium nano-particles on growth, nutrient digestibilities,
www.sciencedirect.com
selected blood parameters and muscle fatty acid profile in broiler chickens. Anim Sci Pap Rep 2014, 32:65-79. c´ık P, Elimam I, Garlı´k J, Bobko M, Tka´c9 ova´ J, Trembecka´ L, 49. Ha9 Ka9 ca´niova´ M: Fatty acid content in broilers Ross 308 meat muscles after using bee pollen and probiotic as supplementary diet into their mixture. Microbiol Biotech Food Sci 2014, 4:67-69. 50. Saleh AA, Hayashi K, Ijiri D, Ohtsuka A: Effect of feeding Aspergillus awamori and canola seed on the growth performance and muscle fatty acid profile in broiler chicken. Anim Sci J 2014, 86:305-311. 51. Bobko M, Ha9 cı´k P, Bobkova´ A, Pavelkova´ A, Tka´c9 ova´ J, Trembecka´ L: Lipid oxidation in chicken meat after application of bee pollen extract, propolis extract and probiotic in their diets. Potravinarstvo 2015, 9:342-346. In the experiment, the effect of the addition of bee pollen, propolis extract and probiotic in a feed mixture for chicken broilers on oxidative stability of breast and thigh muscles during chilled storage was investigated. Results achieved showed that the addition of propolis extract in feed mixture for broiler chickens had positive impact on the reduction of oxidative processes in the breast and thigh muscles during chilling storage, but with the addition of bee pollen extract and probiotic, significant effect on the oxidation of fat in the breast and thigh muscles of meat broiler chickens has been recorded. 52. Kim HW, Yan FF, Hu JY, Cheng HW, Kim YH: Effects of probiotics feeding on meat quality of chicken breast during postmortem storage. Poult Sci 2016, 95:1457-1464. 53. Pieniz S, Andreazza R, Anghinoni T, Camargo F, Brandelli A: Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 2014, 37:251-256.
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