




































 

 

 
5 

© 2019 Conscientia Beam. All Rights Reserved. 

PROBIOTIC SUPPLEMENTATION IN POULTRY PRODUCTION AS AN ALTERNATIVE 
TO ANTIBIOTIC FEED ADDITIVE   

 

 

 Muhammad  
Waseem Birmani1 
Aamir Nawab2 
Muhammad  
Waseem Ghani3 
Guanghui Li4 
Jiang Wu5 
Wenchao Liu6  
Lilong An7+ 

 

1,2,3,4,5,6,7Department of Livestock Productions and Management, Agricultural 
College, Guangdong Ocean University, Guangdong, China. 

 

 
(+ Corresponding author) 

 ABSTRACT 
 
Article History 
Received: 6 March 2019 
Revised: 8 April 2019 
Accepted: 14 May 2019 
Published: 2 July 2019 
 
 
 

Keywords 
Antibiotics resistant 
Growth promoters 
Probiotics 
Poultry production. 

 
Provision of safe and healthy poultry products to the human being is the prime 
objective of the poultry industry, but one should keep in mind the welfare of animals 
and reverence for the environment. Meat and eggs demand also increasing with the 
increase in world human population. To meet this increasing demand for meat and 
eggs, antibiotics growth promoters were used world widely. After the ban on 
antibiotics growth promoters due to its residual effects on human health, nutritionists 
are focusing on novel growth promoters those without causing productivity loss, or 
product quality has augmented. Therefore, probiotics are a safe alternative to 
antibiotics and its beneficial effects proven from many decades. Live microorganisms 
are used to deliver health benefits to chicken, usually by reestablishing or improving 
the intestinal microbiota. Probiotics have a beneficial effect on weight gain, immunity, 
meat traits and somewhat impact on gut health of poultry. The subject of review paper 
will be worthwhile meant for researchers and poultry nutritionists to advance their 
understanding of alternatives to antibiotics in poultry production without affecting 
performance and the welfare of chicken. 
 

Contribution/Originality: This study is important in regards to antibiotic resistance in human being coming 

from animal products. Antibiotic resistance is one of the biggest public health challenges of our time. Each year so 

many people get an antibiotic-resistant infection, and many people die. Fighting this threat is a public health 

priority that requires a collaborative global approach across sectors. So, this study will give direction to researchers 

and food producers to avoid from antibiotics harmful effects to animals and as well as human being. 

 

1. INTRODUCTION 

Poultry business recognized as one of the rapidly growing section among different agriculture sectors. 

Consumption of meat and eggs is increasing due to easy availability, comparatively reasonable price and also rich in 

entire important nutrients which could cover the deficiencies of essential food amino acids, minerals, and vitamins  

Dhama, et al. [1]; Ajit, et al. [2]. Rinttilä and Apajalahti [3] reported that poultry intestinal health has been 

investigated and studied extensively for the higher production performance of chicken, as the intestine is an 

important site where nutrient absorption takes place. While the gut is the main organ which exposed more to 

pathogens microorganisms after skin [4]. For this purpose, since 1940 antibiotics were used in animal feed as 

Animal Review 
2019 Vol. 6, No. 1, pp. 5-16 
ISSN(e): 2409-6490 
ISSN(p): 2412-3382 
DOI: 10.18488/journal.ar.2019.61.5.16 
© 2019 Conscientia Beam. All Rights Reserved. 

 
 
 

 
 

 

 
 
 
 

https://orcid.org/0000-0001-8018-0133
https://www.doi.org/10.18488/journal.ar.2019.61.5.16


Animal Review, 2019, 6(1): 5-16 

 

 
6 

© 2019 Conscientia Beam. All Rights Reserved. 

growth promoters and for gut health maintenance [5-8]. Antibiotics can improve growth rate [9] but on the other 

hand, resistance to antimicrobial agents is increasing between foodborne microbes that can make difficulties in 

public health remedies [10, 11]. Also, antibiotics also destroy some beneficial microflora of gut which may help in 

feed digestion. Furthermore, antibiotics reduced the growth rate by escalating dysbacteriosis and subclinical 

necrotic enteritis [12].  Started from Sweden in the year 1986, antibiotics were taken out from the diet of poultry, 

and pig world widely [6]. Since 2006, antibiotics usage as an animal feed additive is banned by the European 

Union. Therefore, a need for the development of novel interventions that only target pathogenic microorganisms 

whereas safe for beneficial organisms [13]. Recently nutritionists put their efforts on given that a unique and 

different growth promoter and therapeutic agents for disease prevention as well as for the enhancement of chicken 

immune status to avoid antibiotics harmful residual influences on meat and eggs products [14, 15].  Manufacturing 

probiotic feed and food is a crucial progress area for future practical feed and food industry. Currently, the use of 

probiotics is generating a great deal of interest for improvement in poultry production [16].  

Probiotics have been used for health benefits in animal feed as well as in human diet for several years as 

antibiotics alternative [17]. Both FAO, as well as WHO in 2002, has well accepted that probiotics are viable 

microorganisms those must be safe and sufficient for body function that gives benefit to the health status of both 

animals and humans [18]. Moreover, Hill, et al. [19] also gave statement same as FAO and WHO for probiotics 

definition, but he opined simple grammatical correction that probiotics are living microorganisms when consumed 

by animals in sufficient quantities, will improve animals health and productivity. Probiotics when added into feed 

the gut microflora can also be balanced. Probiotics microorganisms provide benefits to the animals through 

improving intestinal microbial balance and as a result enhancing absorption of nutrients, feed efficiency, the growth 

rate of chicken and economic output of birds [20]. There are so many beneficial and protective effects of probiotics 

such as removing pathogenic bacteria by competitive exclusion. 

Furthermore, the positive use of live microorganisms helps in increasing growth and productive performance, 

egg quality, and composition in layers chicken, improve nutrients digestion and absorption and also maintain the 

chicken health [21-23]. The ultimate noteworthy advantage of probiotics is that in animal products, which 

consumed by humans have no residues and it does not exert any resistance in the human while consuming animals 

products. Also, they have a beneficial impact on the production performance of chicken [24, 25]. Many studies told 

us that probiotics have immunomodulatory effects [26, 27]. Probiotics as an alternative to antibiotics growth 

promoters have become prevalent in the poultry industry because consumers demand meat from animals without 

antibiotics residues [28]. Probiotic species used in chicken were Streptococcus, Bifidobacterium, Lactobacillus, Bacillus, 

Candida, Enterococcus, Saccharomyces, and Aspergillus have a beneficial influence on the weight gain of broilers [29, 

30]. The principal objective of our review paper is to describe the positive effects of probiotics in poultry production 

as an alternative to antimicrobial growth promoters, their mechanism of action, and impact on immunity, meat 

traits, and their selection criteria and also to review their uses in the poultry production. 

 

2. WHY WE NEED AN ALTERNATIVE TO ANTIBIOTICS? 

When the ban on antibiotics growth promoter agents in animals in 2006 by the European Union due to the 

following possible risks to animals as well as to human. 

1. Antimicrobial resistance develops and threatens the actual prevention and treatment of an ever-increasing 

range of infections produced by microorganisms. 

2. Antimicrobial resistance is a serious increasing risk for global public health that necessitates action across 

all societies worldwide. 

3. If antibiotics lose their effectiveness due to resistance come from animal meat consumption, the success in 

the treatment of major diseases would be compromised. 



Animal Review, 2019, 6(1): 5-16 

 

 
7 

© 2019 Conscientia Beam. All Rights Reserved. 

4. Treatment cost of the antimicrobial resistant patient may increase to longer illness duration, extra tests 

and more expensive drugs use [31]. 

Due to the above possible threats to human health from antibiotics, we need an alternative growth promoter for 

poultry production.  

 

3. WHAT IS PROBIOTIC? 

Probiotic is single or multi-cultured alive microorganisms which improve the beneficial indigenous microflora 

of host [32]. Probiotics were first used in 1954 to indicate substances that were required for a healthy life. Rather, 

et al. [33] included the bacterial metabolites and dead bacterial culture in the probiotics definition. They are applied 

in farm animal nutrition to increase weight gains and for the improvement of feed conversion.  Microorganisms 

such as mix cultures of different microbes, fungi especially mushroom and yeast and bacteria have been previously 

used as probiotics. Willis, et al. [34] constantly used fungi myceliated grains colonized as probiotic for broiler 

chicken by the eatable mushrooms shiitake (Lentinula edodes). For the treatment of Eimeria tenella infection in 

chickens, wild mushroom Ganoderma lucidum used Ogbe, et al. [35]. Lee, et al. [36] reported that Saccharomyces 

boulardii yeast also used as a treatment of Eimeria infection in poultry. In poultry for the control of pathogenic 

bacterial infection, yeast (Saccharomyces cerevisiae) and Aspergillus oryzae (fungi) also were used as probiotics  [37]. 

While bacterial species are more frequently used as probiotic than fungal probiotic species. Probiotics also have the 

ability to eliminate many pathogenic bacteria such as Escherichia coli, Staphylococcus aureus, Salmonella typhimurium, 

Clostridium perfringens, and so on Iannitti and Palmieri [38]. Kabir [39] reported, commonly used probiotics 

microbes are intestinal strains mostly, E.coli, Lactobacillus casei, L.helveticus, L.plantarum, L.acidophilus, L.lactis, 

L.salivarius, Enterococcus faecium, E.faecalis, and Bifidobacterium species. 

 

4. SELECTION CRITERIA OF PROBIOTICS 

The probiotics strains selection is based mainly on its potential to confer a health benefit for poultry. For 

achieving beneficial results from the use of probiotics must fulfill the following requirements. Should be 

nonpathogenic and nontoxic to poultry. Exact taxonomic identification of probiotic species must consider. A typical 

inhabitant of the directed species that can survive, colonization and must be resistant to bile, enzymes and other 

gastric juice of host and metabolically active in the targeted site [40]. Bile tolerance in the small intestine is 

important for the survival of lactic acid producing bacteria and also for the functionally active in the intestine [41, 

42]. Can compete with pathogenic microflora of gut for adhesion to the intestinal epithelium. Genetically stable 

that can produce antimicrobial substances to antagonize the pathogenic flora and to regulate the host immune 

response. When added in the poultry feed it must show there required organoleptic and technological properties. A 

concerned strain of probiotic must have stability during manufacturing, storage, and during delivery. It should have 

maximum sustainability at higher populations [40].  

 

5. FORMS OF PROBIOTICS 

Probiotics are presented in different forms for example in liquid, powder, sachets, paste, tablets, gel, and 

granules or capsules and many other different forms [38]. Dry forms of probiotics showed enhanced tolerance 

power to gut environment and higher shelf life during storage. Good viability of probiotic in poultry is available 

with the use of hydroxypropyl methylcellulose phthalate-55 as a tablet matrix [38]. 

 

6. MECHANISMS OF ACTION OF PROBIOTICS 

Probiotics have a number of the mode of actions based on the competitive exclusion of pathogenic bacteria, 

production of antibacterial substances and organic acids production for inhibition of all pathogens Mazmanian, et al. 

[43];  Tiwari, et al. [44]. Roselli, et al. [45] proposed that probiotics can moreover govern the anti-inflammatory 



Animal Review, 2019, 6(1): 5-16 

 

 
8 

© 2019 Conscientia Beam. All Rights Reserved. 

cytokines production. Probiotics have the ability to regulate and maintain the intestinal barrier functions and gut 

microbiota homeostasis, Salminen, et al. [46] regulate the gut enzymatic activity and absorption of essential 

nutrients Hooper, et al. [47]; Timmerman, et al. [48] also Gill [49] studied that it prevents procarcinogenic 

enzymes activity and also interfere with pathogens to inhabit and infect the gut mucosa. Furthermore, probiotics 

have the ability to improve the protein as well as some minerals like calcium, iron, manganese, and copper 

absorption from the gut by making acidic pH of the intestine; regulate the production of mucous, regulate epithelial 

functions and increase intestinal motility [50]. Also act as an immunomodulator [51] as probiotics exert effects on 

host antigen presenting cells, regulatory T cells, effector B and T cells, and enterocytes as well [52]. Probiotic can 

activate various immune cells and exert immunomodulatory effect by affecting the T-helper cells in a specific 

manner [53]. Probiotic bacteria can also lessen the cardiovascular diseases risk by lowering blood cholesterol levels 

of the host animal [54]. Unraveled antiviral potential of probiotic bacteria (Lactobacillus Plantarum YML009) 

against H1N1 influenza virus was demonstrated by Rather, et al. [33]. Hydrogen peroxide and lactic acid 

production increased in the gut when fed probiotics, as probiotics have the ability to enhance the growth of 

beneficial gram-positive bacteria, lower the number of intestinal pathogenic microbes [14]. 

 

7. ADVANTAGES OF PROBIOTIC FOR POULTRY 

There are so many beneficial properties of probiotics for poultry proposed by Piva [55]; Jenkins, et al. [56]; 

Simmering and Blaut [57]. 

1. Have the ability to modify intestinal microbiota of chicken 

2. The stimulatory effect on the immune system of chicken 

3. Reduce inflammatory reactions in the host 

4. Prevent pathogen colonization in the intestine 

5. Enhance the performance of animal 

6. Have the ability to lessening the carcass contamination 

7. Lower the blood cholesterol level observed beneficial for chicken 

8. It decreases the ammonia and urea excretion from the chicken 

 

8. EFFECT OF PROBIOTICS ON WEIGHT GAIN  

Many studies revealed that probiotics supplementation to poultry has a constructive influence on chicken 

health and performance. Improved performance of broiler and reduced level of blood cholesterol were seen with the 

supplementation of the probiotic (Pediococcus acidilactici). Significant improvement in daily weight gain and in 

carcass yield was observed in experimental birds than control during all study periods of 6 weeks in both vaccinated 

and non-vaccinated birds [30, 58, 59]. The addition of milk kefir about 2% as prebiotics in meat-type chickens 

drinking water would increase growth performance of broilers, and it may also be supplemented in the chicken feed. 

For achieving the best performance of poultry, only optimum probiotics level was better than an increase in doses 

(quantity) of probiotics [60]. Reduction in the requirements of protein as well as essential amino acids was 

observed when spores of Bacillus subtilis used as probiotics feed additive and as a result, the cost of production for 

per kilogram weight gain can be decreased Mojtaba, et al. [61]. Rajput, et al. [62] reported that the addition of 

Saccharomyces boulardii and Bacillus subtilis as probiotics bring improvement in chicken to live body weight, increases 

bursa of fabricius, as well as thymus weight. Also, it was reported that a significant improvement observed in 

weight gain and the weight of thymus and bursa of fabricius in probiotics fed groups [60].  

 

9. EFFECT OF PROBIOTICS IN IMMUNOMODULATION  

In addition on the way to the improvement in production performance, probiotics also enhance immunity 

against Salmonella challenge without adverse effects on kidney functions in broiler chicks observed by Dina, et al. 



Animal Review, 2019, 6(1): 5-16 

 

 
9 

© 2019 Conscientia Beam. All Rights Reserved. 

[27].  Newcastle antibody titers were significantly higher in broiler chicken fed probiotics as a supplement in the 

diet as compared to control group Rowghani, et al. [63].  Alkhalf, et al. [60] investigate that at 28 and 42 days of 

age the thymus relative weight was greater in all supplemented groups than the control group which leads to an 

increase in lymphocytes numbers in the primary lymphoid organs of the chicken. Spleen weight was observed 

greater for the probiotics fed chickens than the control group [64]. Moreover, the relative weight of bursa was 

improved and increased number of medullar follicles found in the probiotics fed groups as compared to control 

groups of animals [65]. Increase in the bursal relative weight could be a primary positive indication for immunity 

improvement in meat-type chickens [66]. Clostredium butyricum when given as a supplement in the feed as 

probiotics produce large amounts of short-chain fatty acids, such as butyrate and acetate [67] which are an energy 

resource for animals and exert proliferative effects on colonocytes [68]. In broiler chickens improved immunity and 

balance in intestinal microbiota was observed when chicken fed with C. butyricum as a probiotic Yang, et al. [69]. 

Midilli, et al. [70] investigated that the antibody-mediated immune response was higher in probiotic-fed animals 

group. Moreover, presentation of immune-related T helper cells was higher due to probiotic supplementation in 

diet [71]. These above findings were confirmed and elaborated by  Koenen, et al. [24] when they use probiotics 

and investigated that these special effects were mediated by cytokines which secreted by immune cells and this 

process were stimulated by probiotics. 

 

10. EFFECT OF PROBIOTICS ON GUT HEALTH 

We find after a brief review of the literature that probiotics have very limited effects on the core physiological 

functions (digestion, absorption, and propulsion) of the digestive tract of poultry. The strengthening of the 

intestinal mucosal barrier against harmful agents is the major function of probiotics. However, the increase in 

jejunal goblet cells, jejunal and ileal villus height and width were improved when giving Saccharomyces boulardii and 

Bacillus subtilis in the diet. The findings of Rajput, et al. [62] revealed that, an increase in jejunal immunoglobulins 

(IgA-positive) cell numbers in probiotic fed animal groups. It has been stated that probiotics species those have 

more influence on the modulation of gut microbes and the inhibition of pathogenic microbiome are  Saccharomyces, 

Aspergillus, Bacillus, Candida, Streptococcus, Bifidobacterium, Enterococcus, and Lactobacillus [25, 72]. The pathogenic 

microbes inhibition could be somewhat because of the acidic pH of the gut. The decrease in pH is due to the 

breakdown of carbohydrates by probiotics bacteria in the gut which consequently produces volatile fatty acids as 

well as lactic acid and succinic acid some time, and these acids production in gut ultimately reduces the pH of the 

intestine [73]. It is recommended that probiotics supplementation in poultry make a valuable contribution as they 

do not require a withdrawal period. 

 

11. PROBIOTICS EFFECTS ON CHICKEN MEAT TRAITS 

For meat processing and storage physicochemical properties (pH, color, texture, etc.) are much important. As 

these physicochemical properties are interconnected and could affect the meat quality. For processing and storage 

of meat, meat color and pH of meat is an important trait of meat quality, and these both traits together should be 

considered for meat quality evaluation [74]. Above mention traits are closely linked to water holding capacity of 

meat, it is another significant characteristic of meat. When Bacillus subtilis fed to broiler chickens and meat from 

these chickens was stored for 7 days, during storage the significant decreased in pH was observed and this lower pH 

is beneficial for meat storage [75]. Significantly increase in the breast meat redness was observed when 

Lactobacillus fermentum was added in broiler drinking water as probiotics  [76]. And the redness in meat is most 

favored by consumers [77]. However, the other experiment of Haščík, et al. [78] revealed the significant increases 

in the lightness of thigh and breast meat cuts and also increased in yellowness and redness in thighs cuts when 

supplementation of probiotic used in mixture with bee pollen in the broiler. Overall meat sensory attributes were 

evaluated and described that supplementation of probiotics in broiler chicken diet enhanced the meat quality and 



Animal Review, 2019, 6(1): 5-16 

 

 
10 

© 2019 Conscientia Beam. All Rights Reserved. 

microbiological values through the pre-freezing as well as post freezing meat storage [79]. The total viable 

bacterial count was lower for meat obtained from probiotic fed chickens as compared to the meat of control birds. 

Also, quality traits of the meatballs appearance, juiciness, texture, and wholesome acceptability were significantly 

higher in probiotic fed birds while for flavor were lower in probiotics fed birds [80]. On the other hand, improved 

tenderness and overall quality of meat reported when fed cell components of Saccharomyces cerevisiae as probiotics by 

[81]. Tenderness of poultry, as well as other livestock meat, might be made better by supplementing the whole 

yeast or yeast extract from Saccharomyces cerevisiae. 

 

12. EFFECT OF PROBIOTICS ON THE OXIDATION OF LIPID IN MEAT 

Lipid oxidation is a very important deteriorating factor of meat quality and also for other food quality. Lipid 

oxidation commonly complemented via the development of negative changes in odors and flavors. Fatty acids 

composition of meat, linked with the nutritional value of meat is a key component of meat quality. Different studies 

revealed that the fatty acids profile of meat positively affected by probiotics feeding, a major positive effect was the 

reduction of saturated fatty acids contents and an increase in polyunsaturated fatty acids in meat. When Aspergillus 

awamori and Saccharomyces cerevisiae used separately or in a combination in broiler diet, the significant reduction in 

saturated fatty acids profile and increase in polyunsaturated fatty acid in meat was observed [82]. The 

thiobarbituric acid reactive substances (TBARS-test) profile is usually a measure of oxidation in food and also in 

meat. Significantly decreased content of TBARS in breast broiler was observed those fed probiotic (Aspergillus 

awamori and Aspergillus niger). Also increased tocopherol level in muscle was observed and led to low lipid oxidation 

in the experimental groups Saleh, et al. [83]. Abdurrahman, et al. [84] studied that probiotics showed significant 

antioxidant activity observed in both in-vitro as well as in-vivo trials.  

 

13. CONCLUSION 

The demand for antibiotics free residues meat and eggs are probably increasing with the increase in world 

population and advancement in technology. Therefore, to cope with the increasing meat and food demands we need 

more proficient and fast methods. Even though still probiotics are not well established in animal diet, but probiotics 

are a much better alternative to antibiotics in poultry production as probiotics have ability to improving poultry 

intestinal microflora, nutrients utilization, immune response and so on. With the advancement in research and 

technology, we have a list of probiotics species that have a beneficial impact on the animal as well as on a human. 

While the implementation of probiotics as an alternative growth promoter is not well developed in poultry 

production, with research advancement, probiotics will grow into an effective means for the antibiotics free residues 

meat and eggs production. Further research on the beneficial impact of probiotics as antibiotics alternative will 

definitely advantage for all poultry producers countries. 

 

Funding: This study received no specific financial support.    
Competing Interests: The authors declare that they have no competing interests.  
Contributors/Acknowledgement: All authors contributed equally to the conception and design of the 
study. 

 

REFERENCES 

[1] K. Dhama, R. Tiwari, R. U. Khan, S. Chakraborty, M. Gopi, K. Karthik, M. Saminathan, P. A. Desingu, and L. T. 

Sunkara, "Growth promoters and novel feed additives improving poultry production and health, bioactive principles 

and beneficial applications: The trends and advances- A review," International Journal of Pharmacology, vol. 10, pp. 129-

159, 2014. Available at: https://doi.org/10.3923/ijp.2014.129.159. 



Animal Review, 2019, 6(1): 5-16 

 

 
11 

© 2019 Conscientia Beam. All Rights Reserved. 

[2] S. Y. Ajit, K. Gautham, G. Marappan, K. Kumaragurubaran, S. M. Yashpal, and K. D., "Exploring alternatives to 

antibiotics as health-promoting agents in poultry- a review," Journal of Experimental Biology and Agricultural Sciences, 

vol. 4, pp. 368-383, 2016. Available at: https://doi.org/10.18006/2016.4(3s).368.383. 

[3] T. Rinttilä and J. Apajalahti, "Intestinal microbiota and metabolites—Implications for broiler chicken health and 

performance," Journal of Applied Poultry Research, vol. 22, pp. 647-658, 2013. Available at: 

https://doi.org/10.3382/japr.2013-00742. 

[4] M. Yegani and D. Korver, "Factors affecting intestinal health in poultry," Poultry Science, vol. 87, pp. 2052-2063, 2008. 

Available at: https://doi.org/10.3382/ps.2008-00091. 

[5] H. Gaskins, C. Collier, and D. Anderson, "Antibiotics as growth promotants: Mode of action," Animal biotechnology, vol. 

13, pp. 29-42, 2002. 

[6] J. Dibner and J. Richards, "Antibiotic growth promoters in agriculture: History and mode of action," Poultry Science, 

vol. 84, pp. 634-643, 2005. Available at: https://doi.org/10.1093/ps/84.4.634. 

[7] T. Niewold, "The nonantibiotic anti-inflammatory effect of antimicrobial growth promoters, the real mode of action? A 

hypothesis," Poultry Science, vol. 86, pp. 605-609, 2007. Available at: https://doi.org/10.1093/ps/86.4.605. 

[8] N. Eckert, J. Lee, D. Hyatt, S. Stevens, S. Anderson, P. Anderson, R. Beltran, G. Schatzmayr, M. Mohnl, and D. 

Caldwell, "Influence of probiotic administration by feed or water on growth parameters of broilers reared on medicated 

and nonmedicated diets," Journal of Applied Poultry Research, vol. 19, pp. 59-67, 2010. Available at: 

https://doi.org/10.3382/japr.2009-00084. 

[9] A. Nisha, "Antibiotic residues-a global health hazard," Veterinary World, vol. 2, pp. 375-377, 2008. Available at: 

https://doi.org/10.5455/vetworld.2008.375-377. 

[10] H. L. DuPont, "The growing threat of foodborne bacterial enteropathogens of animal origin," Clinical Infectious 

Diseases, vol. 45, pp. 1353-1361, 2007. Available at: https://doi.org/10.1086/522662. 

[11] B. S. Seal, H. S. Lillehoj, D. M. Donovan, and C. G. Gay, "Alternatives to antibiotics: A symposium on the challenges 

and solutions for animal production," Animal Health Research Reviews, vol. 14, pp. 78-87, 2013. Available at: 

https://doi.org/10.1017/s1466252313000030. 

[12] I. Palamidi, K. Fegeros, M. Mohnl, W. Abdelrahman, G. Schatzmayr, G. Theodoropoulos, and K. Mountzouris, 

"Probiotic form effects on growth performance, digestive function, and immune related biomarkers in broilers," Poultry 

science, vol. 95, pp. 1598-1608, 2016. Available at: https://doi.org/10.3382/ps/pew052. 

[13] National Academy of Sciences, "Treating infectious diseases in a microbial world: Report of two workshops on novel 

antimicrobial therapeutics. Washington, D.C.," p. 10. Available: https://www.nap.edu/read/11471/chapter/1, 2006. 

[14] Y. Yang, P. Iji, and M. Choct, "Dietary modulation of gut microflora in broiler chickens: A review of the role of six 

kinds of alternatives to in-feed antibiotics," World's Poultry Science Journal, vol. 65, pp. 97-114, 2009. Available at: 

https://doi.org/10.1017/s0043933909000008. 

[15] A. S. Yadav, G. Kolluri, M. Gopi, K. Karthik, Y. S. Malik, and K. Dhama, "Exploring alternatives to antibiotics as 

health promoting agents in poultry—a review," Journal of Experimental Biology and Agriculture Sciences, vol. 4, pp. 368–

383, 2016. Available at: https://doi.org/10.18006/2016.4(3s).368.383. 

[16] H. Shweta and I. D. Sanjida, "Production of the best natural health supplements using fruit waste materials," 

International Journal of InnovativeRresearch & Development, vol. 3, pp. 131-133, 2014. 

[17] M. J. Zorriehzahra, S. T. Delshad, M. Adel, R. Tiwari, K. Karthik, K. Dhama, and C. C. Lazado, "Probiotics as 

beneficial microbes in aquaculture: an update on their multiple modes of action: A review," Veterinary Quarterly, vol. 36, 

pp. 228-241, 2016. Available at: https://doi.org/10.1080/01652176.2016.1172132. 

[18] FAO/WHO, "Guidelines for the evaluation of probiotics in food," London, Ontario, Canada: Food and Agriculture 

Organization of the United Nations and World Health Organization Working Group Report; 20022002. 

[19] C. Hill, F. Guarner, G. Reid, G. R. Gibson, D. J. Merenstein, B. Pot, L. Morelli, R. B. Canani, H. J. Flint, and S. 

Salminen, "Expert consensus document: The international scientific association for probiotics and prebiotics consensus 

http://www.nap.edu/read/11471/chapter/1


Animal Review, 2019, 6(1): 5-16 

 

 
12 

© 2019 Conscientia Beam. All Rights Reserved. 

statement on the scope and appropriate use of the term probiotic," Nature reviews Gastroenterology & hepatology, vol. 11, 

pp. 506-514, 2014. Available at: https://doi.org/10.1038/nrgastro.2014.66. 

[20] M. Abd El-Hack, S. Mahgoub, M. Alagawany, and E. Ashour, "Improving productive performance and mitigating 

harmful emissions from laying hen excreta via feeding on graded levels of corn DDGS with or without Bacillus subtilis 

probiotic," Journal of Animal Physiology and Animal Nutrition, vol. 101, pp. 904-913, 2017. Available at: 

https://doi.org/10.1111/jpn.12522. 

[21] M. M. Ritzi, W. Abdelrahman, M. Mohnl, and R. A. Dalloul, "Effects of probiotics and application methods on 

performance and response of broiler chickens to an Eimeria challenge," Poultry Science, vol. 93, pp. 2772-2778, 2014. 

Available at: https://doi.org/10.3382/ps.2014-04207. 

[22] M. Alagawany, M. E. A. El-Hack, M. Arif, and E. A. Ashour, "Individual and combined effects of crude protein, 

methionine, and probiotic levels on laying hen productive performance and nitrogen pollution in the manure," 

Environmental Science and Pollution Research, vol. 23, pp. 22906-22913, 2016. Available at: 

https://doi.org/10.1007/s11356-016-7511-6. 

[23] T. Popova, "Effect of probiotics in poultry for improving meat quality," Current Opinion in Food Science, vol. 14, pp. 72-

77, 2017. Available at: https://doi.org/10.1016/j.cofs.2017.01.008. 

[24] M. E. Koenen, J. Kramer, R. Van Der Hulst, L. Heres, S. H. M. Jeurissen, and W. J. A. Boersma, "Immunomodulation 

by probiotic Lactobacilli in layer- and meat-type chickens," British Poultry Science, vol. 45, pp. 355-366, 2004. Available 

at: https://doi.org/10.1080/00071660410001730851. 

[25] K. Mountzouris, P. Tsirtsikos, E. Kalamara, S. Nitsch, G. Schatzmayr, and K. Fegeros, "Evaluation of the efficacy of a 

probiotic containing lactobacillus, bifidobacterium, enterococcus, and pediococcus strains in promoting broiler 

performance and modulating cecal microflora composition and metabolic activities," Poultry Science, vol. 86, pp. 309-

317, 2007. Available at: https://doi.org/10.1093/ps/86.2.309. 

[26] Y. Yurong, S. Ruiping, Z. Shimin, and J. Yibao, "Effect of probiotics on intestinal mucosal immunity and ultrastructure 

of cecal tonsils of chickens," Archives of Animal nutrition, vol. 59, pp. 237–246, 2005. Available at: 

https://doi.org/10.1080/17450390500216928. 

[27] M. W. Dina, S. El-hamd., and M. A. Hams, "Effect of probiotic on Salmonella Enteritidis infection on broiler chickens," 

Egypt.J Chem Environ Health, vol. 2, pp. 298-314, 2016. 

[28] N. V. Christine, C. Wen-Ko, M. H. Billy, R. B. Luc, and R. B. Lisa, . , "Role of probiotics on immune function and their 

relationship to antibiotic growth promoters in poultry. A brief review," International Journal of Probiotics and Prebiotics, 

vol. 11, pp. 1-6, 2016. 

[29] K. S. M. Lutful, "The role of probiotics in the poultry industry," International Journal of Molecular Science, vol. 10, pp. 

3531-3546, 2009. 

[30] A. Ashayerizadeh, N. Dabiri, O. Ashayerizadeh, K. H. Mirzadeh, H. Roshanfekr, and M. Mamooee, "Effect of dietary 

antibiotic, probiotic and prebiotic as growth promoters, on growth performance, carcass characteristics and 

hematological indices of broiler chickens," Pakistan Journal of Biological Sciences, vol. 12, pp. 52-57, 2009. Available at: 

https://doi.org/10.3923/pjbs.2009.52.57. 

[31] A. Awad, N. Arafat, and M. Elhadidy, "Genetic elements associated with antimicrobial resistance among avian 

pathogenic Escherichia coli," Annals of Clinical Microbiology and Antimicrobials, vol. 15, pp. 1-8, 2018. Available at: 

https://doi.org/:10.1186/s12941-016-0174-9. 

[32] G. S. Ghadban, "Probiotics in broiler production-A review," Arch. For Poultry Science, vol. 66, pp. 49-58, 2002. 

[33] I. A. Rather, K. H. Choi, V. K. Bajpai, and Y. H. Park, "Antiviral mode of action of Lactobacillus plantarum YML009 

on Influenza virus H1N1," Bangladesh Journal of Pharmacology, vol. 10, pp. 475–482, 2015. Available at: 

https://doi.org/10.3329/bjp.v10i2.23068. 



Animal Review, 2019, 6(1): 5-16 

 

 
13 

© 2019 Conscientia Beam. All Rights Reserved. 

[34] W. L. Willis, O. S. Isikhuemhen, S. Hurley, and E. I. Ohimain, "Effect of phase feeding of fungus Myceliated grain on 

oocyst excretion and performance of boiler chicken," International Journal of  Poultry Science, vol. 10, pp. 1-3, 2011. 

Available at: https://doi.org/10.3923/ijps.2011.1.3. 

[35] A. O. Ogbe, S. E. Atwod, P. A. Abdu, A. Sannusi, and A. E. Itodo, "Changes in weight gain, facal oocyst count and 

packed cell volume of Eimereria tenella infected broiler treated with a wild mushroom (Gahoderma lucidum) aqueous 

extract," Journal of The South African Veterinary Association, vol. 80, pp. 97-102, 2009. Available at: 

https://doi.org/10.4102/jsava.v80i2.179. 

[36] S. H. Lee, H. S. Lillehoj, R. A. Dalloul, D. W. Park, Y. H. Hong, and J. J. Lin, "Effects of Pediococcus-based probiotic 

on coccidiosis in broiler chickens," Poultry Science, vol. 86, pp. 63-66, 2007. 

[37] K. C. Woo, B. Y. Jung, M. K. Lee, and I. K. Paik, "Effects of supplementary Safmannan (beta glucan and MOS) and 

World-Las (multiple probiotics) on the performance, nutrient availability, small intestinal microflora and immune 

response in broiler chicks," Korean Journal of Poultry Science, vol. 33, pp. 151-158, 2006. 

[38] T. Iannitti and B. Palmieri, "Therapeutical use of probiotic formulations in clinical practice," Clinical Nutrition, vol. 29, 

pp. 701-725, 2010. Available at: https://doi.org/10.1016/j.clnu.2010.05.004. 

[39] S. Kabir, "The role of probiotics in the poultry industry," International Journal of Molecular Sciences, vol. 10, pp. 3531-

3546, 2009. Available at: https://doi.org/10.3390/ijms10083531. 

[40] G. Francesca, P. Mattarelli, and B. Biavati, "Probiotics and prebiotics in animal feeding for safe food production," 

International Journal of Food Microbiology, vol. 141, pp. S15-S28, 2010. Available at: 

https://doi.org/10.1016/j.ijfoodmicro.2010.02.031. 

[41] S. A. Ibrahim and A. Benzkorovainy, "Survival of bifidobacterial in the presence of bile salts," Journal of the science of 

Food and Agriculturec, vol. 62, pp. 351-354, 1993. 

[42] H. S. Park, S. H. Lee, and T. B. Uhm, "Selection of microorganism for probiotics and their characterization," The 

Korean Journal of Food and Nutrition, vol. 27, pp. 433-440, 1998. 

[43] S. K. Mazmanian, J. L. Round, and D. L. Kasper, "A microbial symbiosis factor prevents intestinal inflammatory 

disease," Nature, vol. 453, pp. 620-625, 2008. Available at: https://doi.org/10.1038/nature07008. 

[44] G. Tiwari, R. Tiwari, S. Pandey, and P. Pandey, "Promising future of probiotics for human health: Current scenario," 

Chronicles of Young Scientists, vol. 3, pp. 17-28, 2012. Available at: https://doi.org/10.4103/2229-5186.94308. 

[45] M. Roselli, A. Finamore, M. S. Britti, P. Bosi, I. Oswald, and E. Mengheri, "Alternatives to in-feed antibiotics in pigs: 

Evaluation of probiotics, zinc or organic acids as protective agents for the intestinal mucosa. A comparison of in vitro 

and in vivo results," Animal Research, vol. 54, pp. 203-218, 2005. Available at: 

https://doi.org/10.1051/animres:2005012. 

[46] S. Salminen, E. Isolauri, and E. Salminen, "Clinical uses of probiotics for stabilizing the gut mucosal barrier: successful 

strains and future challenges," Antonie Van Leeuwenhoek, vol. 70, pp. 347-358, 1996. Available at: 

https://doi.org/10.1007/bf00395941. 

[47] L. V. Hooper, T. Midtvedt, and J. I. Gordon, "How host-microbial interactions shape the nutrient environment of the 

mammalian intestine," Annual Review of Nutrition, vol. 22, pp. 283-307, 2002. 

[48] H. Timmerman, L. Mulder, H. Everts, D. Van Espen, E. Van Der Wal, G. Klaassen, S. Rouwers, R. Hartemink, F. 

Rombouts, and A. Beynen, "Health and growth of veal calves fed milk replacers with or without probiotics," Journal of 

Dairy Science, vol. 88, pp. 2154-2165, 2005. Available at: https://doi.org/10.3168/jds.s0022-0302(05)72891-5. 

[49] H. S. Gill, "Probiotics to enhance anti-infective defences in the gastrointestinal tract," Best Practice & Research Clinical 

Gastroenterology, vol. 17, pp. 755-773, 2003. Available at: https://doi.org/10.1016/s1521-6918(03)00074-x. 

[50] S. Raghuwanshi, S. Misra, and P. S. Bisen, "Indian perspective for probiotics: A review," Indian ournal of Dairy Science, 

vol. 68, pp. 195-205, 2015. 



Animal Review, 2019, 6(1): 5-16 

 

 
14 

© 2019 Conscientia Beam. All Rights Reserved. 

[51] N. H. Salzman, D. Ghosh, K. M. Huttner, Y. Paterson, and C. L. Bevins, "Protection against enteric salmonellosis in 

transgenic mice expressing a human intestinal defensin," Nature, vol. 422, pp. 522-526, 2003. Available at: 

https://doi.org/10.1038/nature01520. 

[52] T. A. Oelschlaeger, "Mechanisms of probiotic actions–a review," International Journal of Medical Microbiology, vol. 300, 

pp. 57-62, 2010. Available at: https://doi.org/10.1016/j.ijmm.2009.08.005. 

[53] F. L. Y. Fong, N. P. Shah, P. Kirjavainen, and H. El-Nezami, "Mechanism of action of probiotic bacteria on intestinal 

and systemic immunities and antigen-presenting cells," International Reviews of Immunology, vol. 35, pp. 179-188, 2016. 

Available at: https://doi.org/10.3109/08830185.2015.1096937. 

[54] M. L. Jones, C. Tomaro-Duchesneau, C. J. Martoni, and S. Prakash, "Cholesterol lowering with bile salt hydrolase-

active probiotic bacteria, mechanism of action, clinical evidence, and future direction for heart health applications," 

Expert Opinion on Biological Therapy, vol. 13, pp. 631-642, 2013. Available at: 

https://doi.org/10.1517/14712598.2013.758706. 

[55] A. Piva, "Non-conventional feed additives," Journal of Animal and Feed Sciences, vol. 7, pp. 143–154, 1998. Available at: 

https://doi.org/10.22358/jafs/69962/1998. 

[56] D. J. A. Jenkins, C. W. C. Kendall, and V. Vuksan, "Inulin oligofructose and intestinal function," The Journal of 

Nutrition, vol. 129, pp. 1431–1433, 1999. Available at: https://doi.org/10.1093/jn/129.7.1431s. 

[57] R. Simmering and M. Blaut, "Pro-and prebiotics–the tasty guardian angels?," Applied Microbiology and Biotechnology, 

vol. 55, pp. 19-28, 2001. Available at: https://doi.org/10.1007/s002530000512. 

[58] R. Kalavathy, N. Abdullah, S. Jalaludin, and Y. Ho, "Effects of Lactobacillus cultures on growth performance, 

abdominal fat deposition, serum lipids and weight of organs of broiler chickens," British Poultry Science, vol. 44, pp. 139-

144, 2003. Available at: https://doi.org/10.1080/0007166031000085445. 

[59] S. Kabir, M. M. Rahman, M. Rahman, M. Rahman, and S. Ahmed, "The dynamics of probiotics on growth performance 

and immune response in broilers," International Journal of Poultry Science, vol. 3, pp. 361-364, 2004. Available at: 

https://doi.org/10.3923/ijps.2004.361.364. 

[60] A. Alkhalf, M. Alhaj, and I. Al-Homidan, "Influence of probiotic supplementation on blood parameters and growth 

performance in broiler chickens," Saudi Journal of Biological Sciences, vol. 17, pp. 219-225, 2010. Available at: 

https://doi.org/10.1016/j.sjbs.2010.04.005. 

[61] Z. Mojtaba, Z. Nahid, R. Mohammad, and P. Sudabeh, "Effect of bacillus? Subtilis spore (GalliPro ® ) nutrients 

equivalency value on broiler chicken performance," Italian Journal of Animal Science, vol. 14, pp. 94-98, 2015. 

[62] I. Rajput, L. Li, X. Xin, B. Wu, Z. Juan, Z. Cui, D. Yu, and W. Li, "Effect of Saccharomyces boulardii and Bacillus 

subtilis B10 on intestinal ultrastructure modulation and mucosal immunity development mechanism in broiler 

chickens," Poultry Science, vol. 92, pp. 956-965, 2013. Available at: https://doi.org/10.3382/ps.2012-02845. 

[63] E. Rowghani, M. Arab, and A. Akbarian, "Effects of a probiotic and other feed additives on performance and immune 

response of broiler chicks," International Journal of Poultry Science, vol. 6, pp. 261-265, 2007. Available at: 

https://doi.org/10.3923/ijps.2007.261.265. 

[64] B. R. Dizaji, A. Zakeri, A. Golbazfarsad, S. Faramarzy, and O. Ranjbari, "Influences of different growth promoters on 

intestinal morphology of broiler chickens," European Journal of Experimental Biology, vol. 3, pp. 32-37, 2013. 

[65] H. Shoeib, "Response of broiler chicks to probiotic (pronifer) supplementation," Assiut Veterinary Medical Journal, vol. 

36, pp. 103-116, 1997. 

[66] C. S. Potten, "Stem cells in gastrointestinal epithelium: Numbers, characteristics and death," Philosophical Transactions 

of the Royal Society of London. Series B: Biological Sciences, vol. 353, pp. 821-830, 1998. Available at: 

https://doi.org/10.1098/rstb.1998.0246. 

[67] S. Nakanishi, K. Kataoka, T. Kuwahara, and Y. Ohnishi, "Effects of high amylose maize starch and Clostridium 

butyricum on metabolism in colonic microbiota and formation of azoxymethane-induced aberrant crypt foci in the rat 



Animal Review, 2019, 6(1): 5-16 

 

 
15 

© 2019 Conscientia Beam. All Rights Reserved. 

colon," Microbiology and Immunology, vol. 47, pp. 951-958, 2003. Available at: https://doi.org/10.1111/j.1348-

0421.2003.tb03469.x. 

[68] D. L. Topping and P. M. Clifton, "Short-chain fatty acids and human colonic function: Roles of resistant starch and 

nonstarch polysaccharides," Physiological Reviews, vol. 81, pp. 1031-1064, 2001. Available at: 

https://doi.org/10.1152/physrev.2001.81.3.1031. 

[69] C. Yang, G. Cao, P. Ferket, T. Liu, L. Zhou, L. Zhang, Y. Xiao, and A. Chen, "Effects of probiotic, Clostridium 

butyricum, on growth performance, immune function, and cecal microflora in broiler chickens," Poultry Science, vol. 91, 

pp. 2121-2129, 2012. Available at: https://doi.org/10.3382/ps.2011-02131. 

[70] M. Midilli, M. Alp, N. Kocabach, O. Muglah, N. Turan, H. Yilmaz, and S. Cakir, "Effects of dietary probiotic and 

prebiotic supplementation on growth performance and serum IgG concentration of broilers," South African Journal of 

Animal Science, vol. 38, pp. 21-27, 2008. Available at: https://doi.org/10.4314/sajas.v38i1.4104. 

[71] B.-L. Chiang, Y. Sheih, L. Wang, C. Liao, and H. Gill, "Enhancing immunity by dietary consumption of a probiotic 

lactic acid bacterium (Bifidobacterium lactis HN019): Optimization and definition of cellular immune responses," 

European Journal of Clinical Nutrition, vol. 54, pp. 849-855, 2000. Available at: https://doi.org/10.1038/sj.ejcn.1601093. 

[72] H. Yaman, Z. Ulukanli, M. Elmali, and Y. Unal, "The effect of a fermented probiotic, the kefir, on intestinal flora of 

poultry domesticated geese (Anser anser)," Journal of Veterinary Medicine, vol. 157, pp. 379-386, 2006. 

[73] T. Sakata, T. Kojima, M. Fujieda, M. Takahashi, and T. Michibata, "Influences of probiotic bacteria on organic acid 

production by pig caecal bacteria in vitro," Proceedings of the Nutrition Society, vol. 62, pp. 73-80, 2003. Available at: 

https://doi.org/10.1079/pns2002211. 

[74] A. Węglarz, "Meat quality defined based on pH and colour depending on cattle category and slaughter season," Czech 

Journal of Animal Science, vol. 55, pp. 548-556, 2010. Available at: https://doi.org/10.17221/2520-cjas. 

[75] N. R. Abdulla, A. N. Mohd Zamri, A. B. Sabow, K. Y. Kareem, S. Nurhazirah, F. H. Ling, A. Q. Sazili, and T. C. Loh, 

"Physico-chemical properties of breast muscle in broiler chickens fed probiotics, antibiotics or antibiotic–probiotic 

mix," Journal of Applied Animal Research, vol. 45, pp. 64-70, 2017. Available at: 

https://doi.org/10.1080/09712119.2015.1124330. 

[76] P. Haščík, L. Trembecká, M. Bobko, J. Čuboň, O. Bučko, and J. Tkáčová, "Evaluation of meat quality after application 

of different feed additives in diet of broiler chickens," Potravinarstvo Slovak Journal of Food Sciences, vol. 9, pp. 174-182, 

2015. Available at: https://doi.org/10.5219/429. 

[77] S. Jiang, Z. Jiang, G. Zhou, Y. Lin, and C. Zheng, "Effects of dietary isoflavone supplementation on meat quality and 

oxidative stability during storage in lingnan yellow broilers," Journal of Integrative Agriculture, vol. 13, pp. 387-393, 

2014. Available at: https://doi.org/10.1016/s2095-3119(13)60386-x. 

[78] P. Haščík, L. Trembecká, M. Bobko, M. Kačániová, O. Bučko, J. Tkáčová, and S. Kunová, "Effect of different feed 

supplements on selected quality indicators of chicken meat," Potravinarstvo Slovak Journal of Food Sciences, vol. 9, pp. 

427-434, 2015. Available at: https://doi.org/10.5219/517. 

[79] S. Kabir, M. Rahman, and M. Rahman, "Potentiation of probiotics in promoting microbiological meat quality of 

broilers," Bangladesh Journal of Agricultural Research, vol. 2, pp. 93-96, 2005. 

[80] P. Mahajan, J. Sahoo, and P. Panda, "Effect of probiotic (Lacto-Sacc) feeding, packaging methods and seasons on the 

microbial and organoleptic qualities of chicken meat balls during refrigerated storage," Journal of Food Science and 

Technology (Mysore), vol. 37, pp. 67-71, 2000. 

[81] A. Zhang, B. Lee, S. Lee, K. Lee, G. An, K. Song, and C. Lee, "Effects of yeast (Saccharomyces cerevisiae) cell 

components on growth performance, meat quality, and ileal mucosa development of broiler chicks," Poultry Science, vol. 

84, pp. 1015-1021, 2005. Available at: https://doi.org/10.1093/ps/84.7.1015. 

[82] A. A. Saleh, K. Hayashi, and A. Ohtsuka, "Synergistic effect of feeding Aspergillus awamori and Saccharomyces 

cerevisiae on growth performance in broiler chickens; Promotion of protein metabolism and modification of fatty acid 



Animal Review, 2019, 6(1): 5-16 

 

 
16 

© 2019 Conscientia Beam. All Rights Reserved. 

profile in the muscle," The Journal of Poultry Science, vol. 50, pp. 242-250, 2013. Available at: 

https://doi.org/10.2141/jpsa.0120153. 

[83] A. A. Saleh, Y. Z. Eid, T. A. Ebeid, T. Kamizono, A. Ohtsuka, and K. Hayashi, "Effects of feeding Aspergillus awamori 

and Aspergillus niger on growth performance and meat quality in broiler chickens," The Journal of Poultry Science, vol. 

48, pp. 201-206, 2011. Available at: https://doi.org/10.2141/jpsa.011019. 

[84] Z. H. Abdurrahman, Y. B. Pramono, and N. Suthama, "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, vol. 41, pp. 

37-44, 2016. Available at: https://doi.org/10.14710/jitaa.41.1.37-44. 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 
Views and opinions expressed in this article are the views and opinions of the author(s), Animal Review shall not be responsible or answerable for any loss, 
damage or liability etc. caused in relation to/arising out of the use of the content. 

 

 


