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REVIEW article

Front. Vet. Sci., 11 February 2022
Sec. Animal Nutrition and Metabolism
Volume 8 - 2021 | https://doi.org/10.3389/fvets.2021.794588

Role of Different Growth Enhancers as Alternative to In-feed Antibiotics in Poultry Industry

Kazi Rafiq1* Muhammad Tofazzal Hossain2 Rokeya Ahmed1 Md. Mehedi Hasan1 Rejaul Islam1 Md. Ismail Hossen3 Sourendra Nath Shaha4 Mohammad Rafiqul Islam3
  • 1Department of Pharmacology, Bangladesh Agricultural University, Mymensingh, Bangladesh
  • 2Department of Microbiology and Hygiene, Bangladesh Agricultural University, Mymensingh, Bangladesh
  • 3Livestock Division, Bangladesh Agricultural Research Council, Dhaka, Bangladesh
  • 4Department of Livestock Services, Dhaka, Bangladesh

The poultry industry has grown so fast alongside the irrational use of antibiotics to maximize profit and make the production cost-effective during the last few decades. The rising and indiscriminate use of antibiotics might result in the deposition of residues in poultry food products and in the development of resistance to these drugs by microorganisms. Therefore, many diseases are becoming difficult to treat both in humans and animals. In addition, the use of low-dose antibiotics as growth enhancer results in antibiotic residues in food products, which have detrimental effects on human health. On the other hand, many studies have shown that antibiotics administered to poultry and livestock are poorly absorbed through the gut and usually excreted without metabolism. These excreted antibiotics eventually accumulate in the environment and enter the human food chain, resulting in the bioaccumulation of drug residues in the human body. In this regard, to find out alternatives is of paramount importance for the production of safe meat and egg. Therefore, in recent years, much research attention was disarticulated toward the exploration for alternatives to antibiotic as in-feed growth enhancers after its ban by the EU. As a result, probiotics, prebiotics, phytobiotics, spirulina, symbiotic, and their combination are being used more frequently in poultry production. Feed additives therefore gained popularity in poultry production by having many advantages but without any residues in poultry products. In addition, numerous studies demonstrating that such biological supplements compete with antimicrobial resistance have been conducted. Therefore, the purpose of this review article was to highlight the advantages of using biological products instead of antibiotics as poultry in-feed growth enhancers to enhance the production performance, reduce intestinal pathogenic bacteria, and maintain gut health, potentiating the immune response, safety, and wholesomeness of meat and eggs as evidence of consumer protection, as well as to improve the safety of poultry products for human consumption.

Introduction

Antimicrobial resistance (AMR) is now widely acknowledged as one of the most important global public health threats. The main reason behind this hazard is the irrational and indiscriminate use of antimicrobial drugs in humans, livestock, and the poultry industry. The poultry industry is now considered as one of the fastest-growing subsector of agriculture and veterinary fields due to the increased consumption of meat and egg, making these easily accessible, with a relatively low cost, and rich in most essential nutrients (1). Because of the ease of usage and low cost, antibiotic growth enhancers (AGPs) have been widely used in poultry production around the world. It has changed intensive poultry production by increasing gut health and reducing subclinical infections while also promoting growth, production, and feed conversion efficiency. Antibiotics in low doses improve gut health by reducing the pathogen load and helps in the prevention of subclinical infection in poultry even in well-managed poultry farms. In addition, antibiotics have a number of advantages, including thickening of the gut, which leads to increased nutrient absorption (2). Antibiotics are now given to broiler chicken at a low dose in order to promote a faster growth (3). In contrast to developed economies, the increasing and indiscriminate use of sub-therapeutic doses of antibiotic has had a negative influence on the balance of the normal inhabitants of the gut microflora, gathering antibiotic residues in tissue as well as developing new strains of drug-resistant pathogenic bacteria by mutation or plasmid-mediated transfer (4). This resistant bacteria population enters into the human body through consumption and handling of meat and eggs contaminated with such pathogens that are resistant to antimicrobial drugs (5). Once exposed, the resistant bacteria (superbugs) colonize the intestinal tract of the hosts, and the gene coding for antibiotic resistance in these bacteria can be transferred to other bacteria in the endogenous microflora of the host species, causing a delay in the intervention of bacterial infection (6). On the other hand, destruction of beneficial microbes by antibiotics makes the birds more susceptible to the development of harmful bacteria and coccidia. Therefore, in 2005, the use of antibiotic in animal feed as growth enhancer was banned by the European Union Commission. Antibiotic resistance is being closely monitored, and the governments of many countries are considering banning antibiotic growth enhancers, resulting in a growing interest in discovering viable antibiotic replacements in both layer and broiler production (7). Meanwhile, many alternative substances have been investigated for their potential to replace antibiotic as in-feed growth enhancers. In this regard, numerous research have been carried out to look for natural agents which mimic the similar beneficial effects of growth enhancers, and a lot of researchers have replaced antibiotics with effective dietary supplements, such as probiotic, pre-biotic, phytobiotic, spirulina, symbiotic, and their combination, which are claimed to enhance growth performance and carcass weight and decrease the mortality rate (7, 8). These natural products and their combination have a positive effect on food conversion ratio (FCR), and their residues have not been stored in poultry product and are proven safe. Besides these, these products improve host gut environment, microbial balance, and immune system, reduce stress response, synthesize vitamins, decrease pH, release bacteriocin, and have antimicrobial activity (914). Using probiotic, phytobiotic, pre-biotic, spirulina, symbiotic, and their combination as feed supplement will open a new door to safe poultry production and economic benefits for farmers and public health (8, 15). Recently, phytogenic feed additives have been successfully used as growth promoter alternatives in feed antibiotics due to their positive impact on growth and the immune system and reduced stress response (16). As any of these natural in-feed additives perform better than AGPs without any side effects, here we desired to increase the usage of these worthy components in order to reduce and overcome the overuse of antibiotics—to be more specific, for the reduction of AMR and for the sustainable safety of poultry production. Therefore, in this article, our motive is to introduce the extensive advantages of probiotic, pre-biotic, phytobiotic, spirulina, symbiotic, and some of their combinations as growth enhancer alternatives to antibiotics. We believed that this review article would definitely be helpful to researchers, pharmacists, veterinarians, the pharmaceutical industry, and poultry producers as a perspective on safe poultry production.

Probiotics

According to FAO/WHO (17), probiotics are “live microorganisms which, when administered in adequate amounts, confer a health benefit on the host.” Lilley and Stillwell (18) first introduced the term “probiotic” to describe the “growth-promoting factors” produced by microorganisms. Probiotics (i) improve gut health, inhibit the growth of pathogens, and reduce mortality; (ii) maintain the equilibrium in gut microbial population, which improves intestinal ecology; (iii) reduce the incidence of diarrhea by preventing digestive upset; (iv) increase the growth rate, weight gain, and productivity by improving fed intake and conversion efficiency; (v) enhance the activity of digestive enzymes, which increases nutrient absorption and reduces plasma cholesterol by regulating lipid metabolism; (vi) synthesize vitamin B complex and produce short-chain fatty acid in the intestine, which could alter the microbial composition in the gut; (vii) reduce stress related to vaccination, antibiotic therapy, temperature, transportation, etc.; (viii) enhance the efficacy of vaccines and help in faster detoxification of mycotoxins; (ix) improve fertility and egg quality, reduce chick mortality, and leave no residues in products; (x) reduce ammonia and fecal water contents, which improves litter quality and decreases environmental pollution; and (xi) are cost-effective, prevent the development of antimicrobial resistant bacteria, and help in the production of safe food for consumers (15, 19). Certain non-pathogenic species of bacteria, fungi, yeasts, or their combination have been used as probiotics. Probiotics can be classified into colonizing species (Lactobacillus sp. Enterococcus sp., and Streptococcus sp.) and free, non-colonizing species (Bacillus sp. and Saccharomyces cerevisiae). The microbes generally used to develop probiotics are Lactobacillus acidophilus, L. sporogenes, L. bulgaricus, L. casei, L. plantarum, L. cellobiosus, L. salivarius, Streptococcus faecium, S. thermophiles, Bacillus coagulans, B. licheniformis, Bifidobacterium bifidum, Saccharomyces cerevisiae, Enterococcus faecium, Torulopsis sp., and Aspergillus oryza, which have beneficial effects on broiler performance (15, 20). Probiotics help the elimination of stress-induced anomalies in the gastrointestinal system, hence restoring normal gut activity (21). Probiotics favor in the production of lactic acid and hydrogen peroxide which are harmful to many pathogens, lowering the oxidation–reduction potential in the gut, which inhibits aerobic pathogens such as Staphylococcus aureus, Escherichia coli, Salmonella Enteritidis, S. Typhimurium, Clostridium perfringens, Listeria monocytogenes, Campylobacter jejuni, Yersinia enterocolitica, Candida albicans, and the coccidian parasites Eimeria sp. (15, 22). The mode of action of probiotics include alteration in intestinal flora, enhancement of growth of non-pathogenic facultative anaerobic and Gram-positive bacteria, suppression of growth of intestinal pathogens, and improvement of digestion and utilization of nutrients (23). The antimicrobial activity of Lactobacillus strains, B. longum, and L. johnsonii was observed against Salmonella, Enteritidis, and Listeria monocytogenes, Campylobacter species, and Clostridium perfringens, respectively (15). Probiotic and competitive exclusion approach methods have been used to control endemic and zoonotic diseases in poultry. Exclusion of competition represents competition for binding sites on the intestinal mucous membranes and thus prevents pathogenic microorganisms from colonizing the digestive tract, and the third way is competition for nutrients (24). Besides these, probiotics also contribute in the improvement of the health status of bird by reducing toxic amine and ammonia accumulation, production of essential digestive enzymes, production of B-complex vitamins, and appetite stimulation (8, 25). Kabir et al. (26) observed significant body weight gain and higher antibody production in vaccinated and non-vaccinated birds fed with probiotics time dependently. Similarly, Khaksefidi and Ghoorchi (27) indicated that the antibody titer in the 50-mg/kg-probiotic-fed group was significantly higher at 5 and 10 days post-immunization compared to the control when sheep red blood cell was injected at 7 and 14 days of age. In addition, Mahajan et al. (28) observed a lower total viable count in the meat of birds when supplemented with probiotic (Lacto-Sacc) as compared to the meat obtained from control birds. On the other hand, Zhang et al. (29) reported that meat tenderness was improved by supplementation with whole yeast or Saccharomyces cerevisiae extract in bird feed. Alam and Ferdaushi (7) reported that probiotic supplementation significantly increased dressed carcass weight, abdominal fat, and breast, thigh, and liver and lower abdominal fat percentage in broiler chicks up to 28 days. A previous report also indicated that the use of probiotics (L. acidophilus and S. faecium) increased moisture, protein, ash, water holding capacity, emulsion capacity, and stability in broiler meats (28). B. licheniformis was also found to have a beneficial effect in improving broiler meat quality (30). Georgieva et al. (31) evaluated a significant feed conversion ratio at the 49th day of age in broiler chicken when supplemented with commercial probiotics (Lacto-Saccaro). Recently Hussein et al. (32) reported that supplementing broiler feed with probiotics and photobiotics, alone or in combination, improves performance and intestinal health in broiler chicks. According to Lukic et al. (33), multi-strain probiotics have a beneficial effect on the host by increasing growth-promoting bacteria, combined with the viable antibiosis of pathogenic bacteria in the intestinal tract. In addition, According to Patel et al. (34), probiotics (Protexin) at 100 g/ton in feed significantly boosted body weight gain and FCR, with no negative effects on feed intake, motility, or carcass characteristics. Moreover, adding probiotics in the feed of laying chickens also enhanced the egg production and improved the egg quality (35). Finally, a sub-therapeutic level of antibiotics used in broiler feed could be replaced by probiotics, as was also reported by Palod and Singh (36).

Prebiotics

In 1995, Gibson and Roberfroid (37) first introduced pre-biotic as a non-digestible food element that improves the microbial balance of the host by selectively stimulating the growth of and/or activating the metabolism of one or a small number of health-promoting bacteria in the digestive tract. They are consisting of short-chain carbohydrates, principally oligosaccharides, such as fructo-oligosaccharides, galacto-oligosaccharides, and inulin (37, 38). A good pre-biotic should be processed easily in a large scale, always palatable as a feed ingredient, which induces systemic effects to improve host health, and must not be hydrolyzed or absorbed in the upper part of the gastrointestinal (GI) tract (19). Prebiotics (i) provide a substrate to beneficial intestinal microorganisms to accelerate the growth rate and/or proliferation; (ii) alter the GI microflora, stimulate the immune system, reduce pathogen invasion, and reduce cholesterol and odor compounds; (iii) improve gut health by balancing the intestinal microbes, promoting enzyme reaction, and reducing products of phenol and ammonia; and (iv) reduce the production cost (19, 3942). Prebiotics are capable of enhancing the growth of beneficial bacteria, such as Bifidobacterium and Lactobacillus, but not pathogens causing gastrointestinal diseases such as C. perfringens (37, 43). Fallah and Rezaei (44) reported that the addition of pre-biotic supplementations to broiler diets improved the growth performance and carcass characteristics and decreased the serum cholesterol level of the broiler chickens at 42 days of age. Prebiotics can be used as a potential alternative to growth-promoting antibiotic by altering the intestinal microbes and the immune system to reduce colonization by pathogens, by enhancing nutrient utilization (amino acid and protein), by improving gut health, and also by improving performance (45). Scholz-Ahrens et al. (46) observed a significant increase in the bioavailability of minerals in the gut. Houshmand et al. (47) observed that prebiotics influenced performance and stocking density, resulting in better feed conversion ratio. In addition, Patterson and Burkholder (48) have reported that pre-biotic supplementation has been shown to improve the health status of the gastrointestinal tract in birds. Recently, Froebel et al. (49) have shown that prebiotics enhance growth performance and reduce human foodborne pathogens in poultry.

Phytobiotics

Phytobiotics are secondary plant metabolites which are natural, less toxic, residue-free, and growth-enhancing feed additives. These are also called phytogenics or botanicals that are composed of natural bioactive substances of plant origin, including alkaloids, glycosides, terpenoids, and phenolics (50). Phytobiotics could be classified as herbs from flowering, non-persistent, and non-woody botanicals or spices from non-leaf parts like fruits, seed, bark, or root, essential oils or extracts, and oleoresins (51). Phytobiotics (i) modify the gut microflora by reducing the number of pathogenic organisms; (ii) improve the performance and digestibility by stimulating salivation, secretion of digestible enzymes, and bile production; (iii) improve the normal intestinal architecture, increase the villus length, and also increase the intestinal surface absorption; and (iv) stimulate the secretion of high amounts of intestinal mucus, consequently alleviating pathogen adhesion and establishing gut microbial eubiosis (5254). Cross et al. (55) found that some plant extracts enhance the digestion and secretion of digestive enzymes and also exhibit antibacterial, antiviral, and antioxidant properties. Supplementing broiler diet with clove and cinnamaldehyde (56), garlic (57), a mixture of garlic, mushroom, and propolis (58), essential oil mixtures of thymol and star anise (59), oregano (60), a blend of carvacrol, cinnamaldehyde, and capsicum oleoresin (61), and ginger extract (62) had been found to enhance the performance parameters, including feed consumption, FCR, and body weight. Due to the high antibacterial activity of medium-chain fatty acids, nutritional antibiotic can be replaced with phytobiotic. Ripon et al. (6) used Galibiotic in broiler feed and found that phytobiotics (Galibiotic at 10 gm/kg) significantly lowered the intestinal pH, total viable count, and total coliform count, with best growth performance. Simultaneously, phytobiotics in broiler diet reduce crop and cecal pH (63). A low pH increases the growth of beneficial microorganism, improves nutrient absorption, and thus improves growth performance (64). On the other hand, phytochemical compounds of phytobiotics act against Gram-positive and Gram-negative bacteria either in in vivo (64, 65) or in in vitro environment (66) and were also found to reduce the severity of Eimeria spp. infection in broilers by alleviation of dropping score and intestinal lesion score and also reducing oocyst shedding (67). Besides these, essential oils of lemon, green tea, and turmeric blend have a great efficacy in reducing the count of S. enteritidis and Campylobacter jejuni on the carcass surface of chicken (68). The Eucalyptus volatile oils also have the ability to relieve broilers from complicated respiratory distress caused by Mycoplasma gallisepticum (69). In addition, an immunomodulatory effect is also induced by phytobiotics through increasing immune cell proliferation, increasing cytokine expression, and elevation of antibody titer (70, 71).

Spirulina

Spirulina refers to common blue-green algae that are a natural source of protein, essential amino acids, essential fatty acids, and minerals (72, 73). It is also rich in thiamin, riboflavin, pyridoxin, vitamin B12, vitamin C, and antioxidant carotenoids and is commonly used as a feed component in broiler and layer diets throughout the world (74). Spirulina (i) increases good growth and feed efficiency when added to chick and broiler diet, (ii) induces the growth of beneficial bacteria in the gut which improve broiler health, (iii) upregulates macrophage phagocytic as well as metabolic pathways, (iv) increases disease resistance potential in chicken, (v) acts as natural color enhancers in meats and eggs, and (vi) enriches meat and eggs with polyunsaturated fatty acids (75). Spirulina helps to improve mineral absorption and nutrient digestion processes and protects the gut from diarrhea (76). Spirulina has antiviral activity and immune stimulatory effects (77). Improvement of performance parameters, like FCR, body weight gain, greater production, and percentage of carcass yield, was observed in the dietary group supplemented with Spirulina platensis compared with the other groups (7883). On the other hand, Saxena et al. (84), Venkataraman et al. (85), and Fathi et al. (86) used different concentrations of spirulina in feed and reported that there was no adverse effect on the performance of chickens and thus could be used as a substitute of other feed additives. Access to spirulina powder in the diet at a level of 1% or in drinking water at 0.25% in Japanese quails had beneficial effects on body weight, weight gain, FCR, and fertility when compared with the control groups (87). The final body weight, weekly body weight gain, and FCR of broilers were significantly higher when fed on 6% Spirulina platensis than those of birds fed on 3% of these algae at 42 days of age (88). Considering egg production, it was shown that the diet with spirulina (1.5, 3.0, 6.0, or 12.0%) of laying birds increases egg production with good quality (74, 78). Spirulina is a good source of pigments like carotenoids and xanthophylls, which improve the intensity of egg yolk color; in quails fed with 1% dietary spirulina, an optimal color of the egg yolk was induced (89). A recent study found that the boiled eggs of the spirulina-treated group exhibited a more accepted yolk color than the control group (90). Ginzberg et al. (91) studied the effect of microalgae on the fatty acid content of eggs and found that spirulina-treated eggs have decreased contents of cholesterol and saturated fatty acid, thus increasing the level of omega-3 polysaturated fatty acids. Layer chicken, with ages of 29 to 40 weeks, supplied with 3 g spirulina/kg feed had a significantly higher egg production, egg weight, and egg mass compared to the control group (92). Less than 1% spirulina added to chicken diets enhanced the defense systems for antigen processing, greater T-cell activity, and increased microbial killing (93). Supplementation of dietary spirulina improves the health conditions, indicating the enhancement of the immune response against diseases (94, 95). Moreover, a supply of spirulina at the level of 0.05% to broiler ration could particularly reduce the adverse effect of mycotoxin on the weight of bursa, thymus, and spleen (96). Previous studies also demonstrated that treatment with spirulina increased the number of leukocytes and recommended such as a feed additive to increase the immunity of infected chicken against the avian influenza (AI) H5N1 virus (97). Spirulina platensis (0.5 and 1 g/kg) and vitamin E (75 mg/kg) in the diet enhanced the total antibody production specific for new castle disease virus (98). Shinde et al. (99) conducted an experiment and reported that the inclusion of 0.06% of spirulina in broiler diet as an herbal feed additive is beneficial in improving the feed consumption and feed conversion efficiency. Our recent studies have shown that spirulina (4 gm spirulina/kg layer feed) has a positive effect on egg production in layer birds, with significantly higher (P < 0.05) total erythrocyte count, hemoglobin concentration, and packed cell volume compared to the control group. Serum total cholesterol and triglyceride were significantly decreased in the spirulina-treated group compared to the control group, whereas the high-density lipoprotein cholesterol was increased (P < 0.01) in the treated group. Finally, our present work explores the prospective use of spirulina to improve the lipid profile, hematological parameters, and egg production in layer birds (100).

Synbiotics

Synbiotics are a mixture of probiotics and prebiotics which ensure the growth of probiotics (101, 102). Synbiotics provide a live culture and feed them to improve the survival, persistence, and better growth of useful organisms in the gut of birds as the specific substrate for fermentation (101103). Fructo-oligosaccharides and bifidobacteria as well as lactitol and lactobacilli are the commonly known combinations of probiotics and prebiotics for use as synbiotics (101). The intestinal microflora plays a crucial role in bird health, and if the equilibrium between beneficial microbes is disrupted, the health and general performance of a bird will be affected. This necessitates further investigation of the effect of food supplementation in the form of prebiotics, which can be supplied to stimulate the establishment of beneficial bacteria in chickens, hence increasing the production. In the diet of chickens, synbiotics were effective in increasing broiler growth (104, 105). Synbiotics were observed to improve the intestinal morphology and the level of nutritional absorption in broiler chickens, resulting in improved performance (106, 107). Only a few research have reported the best ways to use synbiotics in poultry (108). Finding the ideal combination of probiotic and pre-biotic as well as evaluating their synergistic effects for use as prospective synbiotics to maintain proper health requires a lot of attention. Madej et al. (109) found that an in vivo injection of inulin (pre-biotic) combined with the Lactobacillus bacteria altered the development of numerous immunological organs in broilers.

The results from another study showed that the use of synbiotic (Gallipro + immunoval) in poultry diets significantly improved the body weight gain and FCR (110). Panda et al. (111) found that, during the trial period (1–42 days), chicks whose meals included L. sporogenes (as probiotics) gained more daily weight and had a better FCR. Prebiotics such as fructo-oligosaccharides and mannan oligosaccharide have also been shown to boost poultry performance (101, 112). Prebiotics may boost probiotic strain development and cloning; therefore, a probiotic-plus-pre-biotic composition may have more benefits than either of them alone. In addition, Mokhtari et al. (110) also reported that the improvement in growth performance observed in symbiotic treatment can be a proof of this assertion. According to the results obtained by Mokhtri et al. (110), it was found to have many benefits for broiler production by adding various growth stimuli. It is clear that adding synbiotics to poultry diets caused a positive effect on performance and the carcass weight produced (110). In a separate study, Al-Sultan et al. (113) found that, in comparison to prebiotics and organic acids, the symbiotic-supplemented group followed by probiotic-supplemented group had the highest final body weight and time-dependent weight gain, better FCR, and the strongest antibody response to Newcastle disease. Furthermore, when compared to prebiotics and organic acids, synbiotics followed by probiotic treatment enhanced the gut morphology and microbial ecology significantly. Finally, when comparing prebiotics and organic acids as effective growth and health boosters for broilers, it may be proposed that using synbiotics followed by probiotics is preferred.

Combination of Probiotics and Phytobiotics

The combination of probiotics and phytobiotics can have beneficial synergistic effects on the gut microbiota in young chickens (114). In addition, when used in broiler feeding, the combination of probiotics and phytobiotics can improve production performance, FCR, gut ecology, immunity, antioxidant status, and also the quality of meat from broilers (8, 115). In our previous study, the combined use of probiotics and phytobiotics in broiler feed showed a significant influence on growth performance, carcass performance, and the amount of stripping with the highest packed cell volume, hemoglobin concentration, visceral organ weight, and increased total viable count after 28 days (8). Increased body weight and better feed conversion ratio due to the combined use of probiotic and phytobiotics in broiler feeds were also observed in many studies (116118). The probiotics and phytobiotics together promote better intestinal growth and provide more energy for the growth of beneficial bacteria in the gut (114, 119). Increased broiler chicken immunity against Salmonella, E. coli, and C. perfringens infections was also reported in many studies (120, 121). The growth of pathogenic bacteria (E. coli and C. perfringens) in the intestines of broiler chickens was also inhibited (8, 32, 122, 123). The combined probiotics produce lower abdominal fat and reduce the mass of meat cholesterol with increased total phenols, flavonoids, and antioxidant activity of broiler chicken meat (118, 124).

Conclusion

Along with our recently published data and evidences published elsewhere, the use of probiotics, prebiotics, phytobiotics, spirulina, synbiotics, and combinations of probiotic and phytobiotics as growth enhancers/feed additives have many potential benefits, including improved digestion and absorption of nutrients, optimization of feed conversion ratio, growth performance, immunomodulation, and improved gut function and health through the exclusion and inhibition of pathogens in the intestine; thereby, the level of safety of poultry products for human consumption is being improved. However, their effectiveness as growth enhancers is dependent on a number of circumstances, including diet compatibility and the alternatives used, hygiene standards, and sound farm management practices. In this regard, more research is needed to look at other combinations of these alternatives with a specific target relationship between the host and beneficial bacteria as well as a more precise recommended dose to boost layer and broiler production. Furthermore, in light of customer demand for safe meat and eggs as well as attempts to prevent antimicrobial resistance, more options for the use of antibiotics as growth enhancer in poultry production with desirable attributes without compromising the welfare of layer and broiler birds must be explored. Meanwhile, awareness must be raised to prevent the irrational use of antibiotics as an in-feed growth booster or for the prevention of diseases in the poultry industry.

Author Contributions

KR and MT revised and finalized the manuscript. RA, MMH, and RI prepare the draft. MIH, SS, and MI revised and edit the reference section. All authors contributed to the article and approved the submitted version.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

1. Dhama K, Latheef SK, Saminathan M, Samad HA, Karthik K, Tiwari R, et al. Multiple beneficial applications and modes of action of herbs in poultry health and production- a review. Int J Pharma. (2015) 11:152–76. doi: 10.3923/ijp.2015.152.176

PubMed Abstract | CrossRef Full Text

2. Cox CM, Dalloul RA. Immunomodulatory role of probiotics in poultry and potential in ovo application. Benef Microbes. (2015) 6:45–52. doi: 10.3920/BM2014.0062

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Costa MC, Bessegatto JA, Alfieri AA, Weese JS, Filho JAB, Oba A. Different antibiotic growth promoters induce specific changes in the cecal microbiota membership of broiler chicken. PLoS ONE. (2017) 12:e0171642. doi: 10.1371/journal.pone.0171642

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Castanon JIR. History of the use of antibiotic as growth promoters. J Poult Sci. (2007) 86:2466–71. doi: 10.3382/ps.2007-00249

PubMed Abstract | CrossRef Full Text | Google Scholar

5. Van den Bogaard AE, Stobberingh. Epidemiology of resistance to antibiotics. Links between animals and humans. Int J Antimicrob Agents. (2000) 14:327–35. doi: 10.1016/S0924-8579(00)00145-X

PubMed Abstract | CrossRef Full Text | Google Scholar

6. Ripon MMR, Rashid MH, Rahman MM, Ferdous MF, Arefin MS, Sani AA, et al. Dose-dependent response to phytobiotic supplementation in feed on growth, hematology, intestinal pH, and gut bacterial load in broiler chicken. J Adv Vet Anim Res. (2019) 6:253–9. doi: 10.5455/javar.2019.f341

PubMed Abstract | CrossRef Full Text | Google Scholar

7. Alam MJ, Ferdaushi Z. Use of probiotics instead of antibiotics in broiler production. Prog Agric. (2018) 29:359–70. doi: 10.3329/pa.v29i4.41350

PubMed Abstract | CrossRef Full Text | Google Scholar

8. Ferdous MF, Arefin MS, Rahman MM, Ripon MMR, Rashid MH, Sultana MR, et al. Beneficial effects of probiotic and phytobiotic as growth promoter alternative to antibiotic for safe broiler production. J Adv Vet Anim Res. (2019) 6:409–15. doi: 10.5455/javar.2019.f361

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Fuller R. Probiotics in man and animals. J Appl Bacteriol. (1989) 66:365–78. doi: 10.1111/j.1365-2672.1989.tb05105.x

CrossRef Full Text | Google Scholar

10. Nahashon SN, Nakne HS, Mirosh LW. Production variables and nutrient retention in single comb white leghorn laying pullets fed diets supplemented with direct-fed microbials. Poult Sci. (1994) 73:1699–711. doi: 10.3382/ps.0731699

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Rolfe RD. The role of probiotic cultures in the control of gastrointestinal health. J Nutr. (2000) 130:3965–4025. doi: 10.1093/jn/130.2.396S

PubMed Abstract | CrossRef Full Text | Google Scholar

12. Manafi M. Comparison study of a natural non-antibiotic growth promoter and a commercial probiotic on growth performance, immune response and biochemical parameters of broiler chicks. J Poult Sci. (2015) 52:274–81. doi: 10.2141/jpsa.0150027

CrossRef Full Text | Google Scholar

13. Gilani SMH, Zehra S, Hassan F, Galani S, Ashraf A. Effect of natural growth promoters on immunity, and biochemical and haematological parameters of broiler chickens. Trop J Pharm Res. (2018) 17:627–33. doi: 10.4314/tjpr.v17i4.9

CrossRef Full Text | Google Scholar

14. Hafeez A, Ullah Z, Khan RU, Qudrat U, Naz S. Effect of diet supplemented with coconut essential oil on performance and villus histomorphology in broiler exposed to avian coccidiosis. Trop Anim Health Prod. (2020) 52:2499–504. doi: 10.1007/s11250-020-02279-6

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Dhama K, Tiwari R, Khan RU, Chakraborty S, Gopi M, Karthik K, et al. Growth promoters and novel feed additives improving poultry production and health, bioactive principles and beneficial applications: the trends and advances- a review. Int J Pharmacol. (2014) 10:129–59. doi: 10.3923/ijp.2014.129.159

CrossRef Full Text | Google Scholar

16. Mehdi Y, Létourneau-Montminy MP, Gaucher ML, Chorfi Y, Suresh G, Rouissi T, et al. Use of antibiotics in broiler production: global impacts and alternatives. Anim Nutr. (2018) 4:170–8. doi: 10.1016/j.aninu.2018.03.002

PubMed Abstract | CrossRef Full Text | Google Scholar

17. FAO/WHO. Health and Nutritional Properties of Probiotics in Food Including Powder Milk With Live Lactic Acid Bacteria. Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria. Córdoba: FAO/WHO (2001). p. 1–34.

Google Scholar

18. Lilly DM, Stillwell RH. Probiotics: growth promoting factors produced by microorganisms. Science. (1965) 147:747–8. doi: 10.1126/science.147.3659.747

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Yadav AS, Kolluri G, Gopi M, Karthik K, Malik YS, Dhama K. Exploring alternatives to antibiotics as health promoting agents in poultry- a review. J Exp Biol Agric Sci. (2016) 4:368–83. doi: 10.18006/2016.4(3S).368.383

CrossRef Full Text | Google Scholar

20. Ashayerizadeh A, Dabiri N, Ashayerizadeh O, Mirzadeh KH, Roshanfekr H, Mamooee M. Effect of dietary antibiotic, probiotic and prebiotic as growth promoters, on growth performance, carcass characteristics and hematological indices of broiler chickens. Pak J Biol Sci. (2009) 12:52–7. doi: 10.3923/pjbs.2009.52.57

PubMed Abstract | CrossRef Full Text | Google Scholar

21. Kutlu HR, Görgülü M. The alternatives for antibiotics-growth factors used in poultry diets as feed additives. Yem Agazin Dergisi. (2001) 27:45–51.

22. Singh BP, Chauhan RS. Role of probiotics in control of poultry diseases. Pashudhan. (2004) 17:3.

23. Yeo J, Kim KI. Effect of feeding diets containing an antibiotic, a probiotic, or yucca extract on growth and intestinal urease activity in broiler chicks. Poult Sci. (1997) 76:381–5. doi: 10.1093/ps/76.2.381

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Patterson JA, Burkholder KM. Application of prebiotics and probiotics in poultry production. Poult Sci. (2003) 82:627–31. doi: 10.1093/ps/82.4.627

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Dierck NA. Biotechnology aids to improve feed and feed digestion: enzymes and fermentation. Arch Anim Nutr Berl. (1989) 39:241–61. doi: 10.1080/17450398909429530

PubMed Abstract | CrossRef Full Text | Google Scholar

26. Kabir SML, Rahman MM, Rahman MB, Rahman MM, Ahmed SU. The dynamics of probiotics on growth performance and immune response in broilers. Int J Poult Sci. (2004) 3:361–4.

Google Scholar

27. Khaksefidi A, Ghoorchi T. Effect of probiotic on performance and immunocompetence in broiler chicks. J Poult Sci. (2006) 43:296–300. doi: 10.2141/jpsa.43.296

CrossRef Full Text | Google Scholar

28. Mahajan P, Sahoo J, Panda PC. Effect of probiotic (Lacto-Sacc) feeding, packaging methods and season on the microbial and organoleptic qualities of chicken meat balls during refrigerated storage. J Food Sci Technol Mysore. (2000) 37:67–71.

Google Scholar

29. Zhang AW, Lee BD, Lee SK, Lee KW, An GH, Song KB, et al. Effects of yeast (Saccharomyces cerevisiae) cell components on growth performance, meat quality, and ileal mucosa development of broiler chicks. Poult Sci. (2005) 84:1015–21. doi: 10.1093/ps/84.7.1015

PubMed Abstract | CrossRef Full Text | Google Scholar

30. Liu X, Yan H, Lv L, Xu Q, Yin C, Zhang K, et al. Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian Australas J Anim Sci. (2012) 25:683–9. doi: 10.5713/ajas.2011.11334

PubMed Abstract | CrossRef Full Text | Google Scholar

31. Georgieva V, Denev ST, Marinov B. Effect of some probiotic and nutritive means on chicken broiler productivity. Zhivotnovdni Nauki. (2000) 37:19–23.

Google Scholar

32. Hussein EOS, Ahmed SH, Abudabos AM, Aljumaah MR, Alkhlulaifi MM, Nassan MA, et al. Effect of antibiotic, phytobiotic and probiotic supplementation on growth, blood indices and intestine health in broiler chicks challenged with clostridium perfringens. Animals. (2020) 10:507. doi: 10.3390/ani10030507

PubMed Abstract | CrossRef Full Text | Google Scholar

33. Lukic J, Chen V, Strahinic I, Begovic J, Lev-Tov H, Davis SC, et al. Probiotics or pro-healers: the role of beneficial bacteria in tissue repair. Wound Repair Rege. (2017) 25:912–22. doi: 10.1111/wrr.12607

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Patel SG, Raval AP, Bhagwat SR, Sadrasaniya DA, Patel AP, Joshi SS. Effects of probiotics supplementation on growth performance, feed conversion ratio and economics of broilers. J Anim Res. (2015) 5:155. doi: 10.5958/2277-940X.2015.00026.1

CrossRef Full Text | Google Scholar

35. Chung SH, Lee J, Kong C. Effects of multi strain probiotics on egg production and quality in laying hens fed diets containing food waste product. Int J Poult Sci. (2015) 14:19–22. doi: 10.3923/ijps.2015.19.22

CrossRef Full Text | Google Scholar

36. Palod J, Singh VS. Role of probiotics in broiler feeding. In: Sadana's All India Poultry Business Directory (Year Book 2003–2004) Special Millennium issue. 2nd ed. Ghaziabad: Sadana publishers and Distributors (2004). p. 147–8.

37. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota – introducing the concept of prebiotics. J Nutr. (1995) 125:1401–12. doi: 10.1093/jn/125.6.1401

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Panitantum V. The story of probiotics, prebiotics & synbiotics. In: A Seminar Presentation at Kasetsart University, Bangkok. Bangkok: Under the Auspices of BIOTEC, National Science and Technology Development Agency (2004). p. 157–61.

39. Cummings JH, Macfarlane GT. Gastrointestinal effects of prebiotics. Br J Nutr. (2002) 87:S145–51. doi: 10.1079/BJN/2002530

CrossRef Full Text | Google Scholar

40. Ghiyasi M, Rezaei M, Sayyahzadeh MH. Effect of prebiotic (fermacto) in low protein diet on performance and carcass characteristics of broiler chicks. Int J Poult Sci. (2007) 6:661–5. doi: 10.3923/ijps.2007.661.665

CrossRef Full Text | Google Scholar

41. Khaksar V, Golian A, Kermanshahi H, Movasseghi AR, Jamshidi A. Effect of prebiotic fermacto on gut development and performance of broiler chickens fed diet low in digestible amino acids. J Anim Vet Adv. (2008) 7:251–7.

Google Scholar

42. Peric L, Zikic D, Lukic M. Application of alternative growth promoters in broiler production. Biotechnol Anim Husb. (2009) 25:387–97. doi: 10.2298/BAH0906387P

CrossRef Full Text | Google Scholar

43. Kolida S, Tuohy K, Gibson GR. Prebiotic effects of inulin and oligofructose. Br J Nutr. (2002) 87:S193–7. doi: 10.1079/BJN/2002537

CrossRef Full Text | Google Scholar

44. Fallah R, Rezaei H. Effect of dietary prebiotic and acidifier supplementation on the growth performance, carcass characteristics and serum biochemical parameters of broilers. J Cell Anim Biol. (2013) 7:21–4. doi: 10.5897/JCAB12.065

CrossRef Full Text | Google Scholar

45. Hajati H, Rezaei M. The application of prebiotics in poultry production. Int J Poult Sci. (2010) 9:298–304. doi: 10.3923/ijps.2010.298.304

CrossRef Full Text | Google Scholar

46. Scholz-Ahrens KM, Schaafsma G, Van Den Heuvel EGHM, Schre-zenmeir J. Effects of prebiotics on mineral metabolism. Am J Clin Nutr. (2001) 73:459S−64. doi: 10.1093/ajcn/73.2.459s

PubMed Abstract | CrossRef Full Text | Google Scholar

47. Houshmand M, Azhar K, Zulkifli I, Bejo M, Kamyab A. Effects of prebiotic, protein level, and stocking density on performance, immunity, and stress indicators of broilers. Poult Sci. (2012) 91:393–401. doi: 10.3382/ps.2010-01050

PubMed Abstract | CrossRef Full Text | Google Scholar

48. Patterson JA, Burkholder KM. Prebiotic feed additives: rationale and use in pigs. In: Ball RA, editor. Proceedings of the 9th International Symposium on Digestive Physiology in Pigs. Banff, AB: University of Alberta (2003). p. 319–31.

Google Scholar

49. Froebel LK, Jalukar S, Lavergne TA, Lee JT, Duong T. Administration of dietary prebiotics improves growth performance and reduces pathogen colonization in broiler chickens. Poult Sci. (2019) 98:6668–76. doi: 10.3382/ps/pez537

PubMed Abstract | CrossRef Full Text | Google Scholar

50. Shad AA, Ahmad S, Ullah R, AbdEl-Salam NM, Fouad H, Ur Rehman N, et al. Phytochemical and biological activities of four wild medicinal plants. Sci World J. (2014) 2014:857363. doi: 10.1155/2014/857363

PubMed Abstract | CrossRef Full Text | Google Scholar

51. Bote CJL. Bioflavonoid's effects reach beyond productivity. Feed Mix. (2004) 12:12–5.

52. Alcicek A, Bozkurt M, Çabuk M. The effect of a mixture of herbal essential oils, an organic acid or a probiotic on broiler performance. South African J Anim Sci. (2004) 34:217–22.

Google Scholar

53. Alloui N, Alloui MN, Agabou A. Application of herbs and phytogenic feed additives in poultry production - a review. Glob J Anim Sci Res. (2014) 2:234–43.

PubMed Abstract | Google Scholar

54. Tabatabaei SN. Effect of olibanum (Boswellia thurifera) as a feed additive on performance, some blood biochemical and intestinal morphology in broiler chicks. Res Opin Anim Vet Sci. (2016) 6:130–4. doi: 10.20490/ROAVS/16-023

CrossRef Full Text | Google Scholar

55. Cross DE, Mcdevitt RM, Hillman K, Acamovic T. The effect of herbs and their associated essential oils on performance, dietary digestibility and gut microflora in chickens from 7 to 28 days of age. Br Poult Sci. (2007) 48:496–506. doi: 10.1080/00071660701463221

PubMed Abstract | CrossRef Full Text | Google Scholar

56. Chalghoumi R, Belgacem A, Trabelsi I, Bouatour Y, Bergaoui R. Effect of dietary supplementation with probiotic or essential oils on growth performance of broiler chickens. Int J Poult Sci. (2013) 12:538–44. doi: 10.3923/ijps.2013.538.544

CrossRef Full Text | Google Scholar

57. Elagib HAA, El-Amin WIA, Elamin KM, Malik HEE. Effect of dietary garlic (Allium sativum) supplementation as feed additive on broiler performance and blood profile. J Anim Sci Adv. (2013) 3:58–64. doi: 10.5455/jasa.20130219104029

CrossRef Full Text | Google Scholar

58. Daneshmand A, Sadeghi GH, Karimi A. The effects of a combination of garlic, oyster mushroom and propolis extract in comparison to antibiotic on growth performance, some blood parameters and nutrients digestibility of male broilers. Brazilian J Poult Sci. (2012) 14:141–7. doi: 10.1590/S1516-635X2012000200009

CrossRef Full Text | Google Scholar

59. Kim SJ, Lee KW, Kang CW, An BK. Growth performance, relative meat and organ weights, cecal microflora, and blood characteristics in broiler chickens fed diets containing different nutrient density with or without essential oils. Asian Australas J Anim Sci. (2016) 29:549–54. doi: 10.5713/ajas.15.0426

PubMed Abstract | CrossRef Full Text | Google Scholar

60. Hashemipour H, Kermanshahi H, Golian A, Khaksar V. Effects of carboxy methyl cellulose and thymol + carvacrol on performance, digesta viscosity and some blood metabolites of broilers. J Anim Phy Anim Nutr. (2014) 98:672–9. doi: 10.1111/jpn.12121

PubMed Abstract | CrossRef Full Text | Google Scholar

61. Bravo D, Ionescu C. Meta-analysis of the effect of a mixture of carvacrol, cinnamaldehyde and capsicum oleoresin in broilers. Poul Sci. (2008) 87:75.

62. Olaifa RO, Sogunle OM, Obileye LI, Ibitoye SA, Ayodeji TM, Odutayo OJ, et al. Effect of oral administration of three different phytobiotics on growth performance of locally-adapted turkeys. EC Vet Sci. (2019) 4:656–62.

63. Al-Tarazi YH, Alshawabkeh K. Effect of dietary formic and propionic acids on Salmonella pullorum shedding and mortality inlayer chicks after experimental infection. J Vet Med. (2003) 50:112–7. doi: 10.1046/j.1439-0450.2003.00644.x

PubMed Abstract | CrossRef Full Text | Google Scholar

64. Boling SD, Snow JL, Parsons CM, Baker DH. The effect of citric acid on calcium and phosphorus requirements of chicks fed corn-soybean meal diets. Poult Sci. (2001) 80:783–8. doi: 10.1093/ps/80.6.783

PubMed Abstract | CrossRef Full Text | Google Scholar

65. Daka D. Antibacterial effect of garlic (Allium sativum) on Staphyloccus aureus: an in vitro study. African J Biotech. (2013) 10:666–9.

Google Scholar

66. Al-Mariri A, Safi M. In vitro antibacterial activity of several plant extracts and oils against some gram-negative bacteria. Iran J Med Sci. (2014) 39:36–43.

PubMed Abstract | Google Scholar

67. Zyan KA, Elshourbagy MA, Aggour G Abdelfattah MA. Molecular identification of E. tenella in broiler chicks in Kalyoubia governorate and evaluation of different strategies for control cecal coccidiosis. Benha Vet Med J. (2017) 33:175–82. doi: 10.21608/bvmj.2017.43882

CrossRef Full Text | Google Scholar

68. Murali N, Kumar-Phillips GS, Rath NC, Marcy J, Slavik MF. Effect of marinating chicken meat with lemon, green tea and turmeric against food borne bacterial pathogens. Int J Poult Sci. (2012) 11:326–32. doi: 10.3923/ijps.2012.326.332

CrossRef Full Text | Google Scholar

69. Abd El-Ghany WA. Assessment of the efficacy of certain antibiotics and volatile oils for the treatment of induced Mycoplasma gallisepticum infection in broiler chickens. J Egyp Vet Med Assoc. (2008) 68:29–45.

Google Scholar

70. Lee SH, Lillehoj HS, Hong YH, Jang SI, Lillehoj EP, Ionescu C, et al. In vitro effects of plant and mushroom extracts on immunological function of chicken lymphocytes and macrophages. Br Poult Sci. (2010) 51:213–21. doi: 10.1080/00071661003745844

PubMed Abstract | CrossRef Full Text | Google Scholar

71. Park IJ, Cha SY, Kang M, So YS, Go HG, Mun SP, et al. Effect of proanthocyanidin-rich extract from Pinus radiata bark on immune response of specific-pathogen-free white leghorn chickens. Poult Sci. (2011) 90:977–82. doi: 10.3382/ps.2010-01160

PubMed Abstract | CrossRef Full Text | Google Scholar

72. Cheong SH, Kim MY, Sok DE, Wang SYH, Kim JH, Kim HR, et al. Spirulina prevents atherosclerosis by reducing hypercholesterolemia in rabbits fed a high-cholesterol diet. J Nutr Sci Vitaminol. (2010) 56:34–40. doi: 10.3177/jnsv.56.34

PubMed Abstract | CrossRef Full Text | Google Scholar

73. Jafari SMA, Rabbani M, Emtyazjoo M, Piryaei F. Effect of dietary Spirulina platensis on fatty acid composition of rainbow trout (Oncorhynchus mykiss) fillet. Aquacu Inter J. (2014) 22:1307–15. doi: 10.1007/s10499-013-9748-0

CrossRef Full Text | Google Scholar

74. Ross E, Dominy W. The nutritional value of dehydrated, blue-green algae (Spirulina plantensis) for poultry. Poult Sci. (1990) 69:794–800. doi: 10.3382/ps.0690794

PubMed Abstract | CrossRef Full Text | Google Scholar

75. Kumar RSP, Sibi G. Spirulina as poultryfeed supplement to enhance nutritional value of chicken meat and eggs: a review. Int J Microbiol Res. (2020) 11:67–71.

76. GruŽauskas R, Lekavičius R, Racevičiute-Stupeliene A, Šašyte V, Tevelis V, Švirmickas GJ. Viščiuku broileriu virškinimo procesu optimizavimas simbiotiniais preparatais. Vet Irzoote. (2004) 28:51–6.

Google Scholar

77. Khan M, Shobha CJ, Rao UM, Sundaram CM, Singh S, Mohan JI, et al. Protective effect of Spirulina against doxorubicininduced cardio-toxicity. Phytother Res. (2005) 19:1030–7. doi: 10.1002/ptr.1783

PubMed Abstract | CrossRef Full Text | Google Scholar

78. Ross E, Dominy W. The effect of dehydrated Spirulina platensis on poultry. Poult Sci. (1985) 64:173.

79. Evans AM, Smith DL, Moritz JS. Effects of algae incorporation into broiler starter diet formulations on nutrient digestibility and 3 to 21 d bird performance. J Appl Poult Res. (2015) 24:206–14. doi: 10.3382/japr/pfv027

CrossRef Full Text | Google Scholar

80. Nikodémusz E, Páskai P, Tóth L, Kozák J. Effect of dietary Spirulina supplementation on the reproductive performance of farmed pheasants. Techn Art Poult Indust. (2010) 1–2.

81. Kharde S, Shirbhate R, Bahiram K, Nipane S. Effect of Spirulina supplementation on growth performance of broilers. Ind J Vet Res. (2012) 21:66–9.

Google Scholar

82. Mariey Y, Samak H, Abou-Khashba H, Sayed M, Abou-Zeid A. Effect of using Spirulina platensis algae as a feed additives for poultry diets: productive performance of broiler. Egypt Poult Sci. (2014) 34:245–58.

83. Kaoud HA. Effect of Spirulina platensis as a dietary supplement on broiler performance in comparison with prebiotics. J Biol Sci. (2015) 1:1–6.

Google Scholar

84. Saxena PN, Ahmad MR, Shyam R, Amla DV. Cultivation of Spirulina in sewage for poultry feed. Experientia. (1983) 39:1077–83. doi: 10.1007/BF01943117

CrossRef Full Text | Google Scholar

85. Venkataraman LV, Somasekaran T, Becker EW. Replacement value of blue green alga (Spirulina platensis) for fishmeal and a vitamin-mineral premix for broiler chicks. Br Poult Sci. (1994) 35:373–81. doi: 10.1080/00071669408417702

PubMed Abstract | CrossRef Full Text | Google Scholar

86. Fathi MA, Namra MMM, Ragab MS, Aly MMM. Effect of dietary supplementation of algae meal (Spirulina platensis) as growth promoter on performance of broiler chickens. Egypt Poult Sci J. (2018) 38:375–89.

Google Scholar

87. Abouelezz FMK. Evaluation of Spirulina algae (Spirulina platensis) as a feed supplement for Japanese quail: nutritional effects on growth performance, egg production, egg quality, blood metabolites, sperm-egg penetration and fertility. Egyp Poult Sci J. (2017) 37:707–19. doi: 10.21608/epsj.2017.5390

CrossRef Full Text | Google Scholar

88. Abd El-Hady AM, El-Ghalid OAH. Spirulina platensis algae (SPA): a novel poultry feed additive. Effect of SPA supplementation in broiler chicken diets on productive performance, lipid profile and calcium-phosphorus metabolism. Worlds Poult Sci J. (2018) 7498:1–7.

89. Anderson DW, Tang CS, Ross E. The xanthophylls of Spirulina and their effect on egg yolk pigmentation. Poult Sci. (1991) 70:115–9. doi: 10.3382/ps.0700115

CrossRef Full Text | Google Scholar

90. Sujatha T, Narahari D. Effect of designer diets on egg yolk composition of ‘white leghorn’ hens. J Food Sci Technol. (2011) 48:494–7. doi: 10.1007/s13197-010-0132-z

PubMed Abstract | CrossRef Full Text | Google Scholar

91. Ginzberg A, Cohen M, Sod-Moriah UA, Shany S, Rosenshtrauch A, Arad SM. Chickens fed with biomass of the red microalga Porphyridium sp. have reduced blood cholesterol level and modified fatty acid composition in egg yolk. J Appl Phycol. (2000) 12:325–30. doi: 10.1023/A:1008102622276

CrossRef Full Text | Google Scholar

92. Mobarez SM, Rizk AM, Abdel latif AM, Osama AE. Effect of supplementing diet with Spirulina platensis algae or turmeric on productive and reproductive performance of golden montazah layers. Egypt Poult Sci J. (2018) 38:109–25.

PubMed Abstract | Google Scholar

93. Qureshi M, Garlich D, Kidd M, Ali R. Immune enhancement potential of Spirulina platensis in chickens. Poult Sci. (1994) 73:46.

94. Baojiang G. Study on effect and mechanism of polysaccharides of Spirulina on body immune function improvement. In: Second Asia-Pacific Conference on Algal Biotechnology, Sentosa. Singapore (1994).

95. Holman BWB, Malau-aduli AEO. Spirulina as a livestock supplement and animal feed. J Anim Physiol Anim Nutr. (2012) 97:615–23. doi: 10.1111/j.1439-0396.2012.01328.x

PubMed Abstract | CrossRef Full Text | Google Scholar

96. Raju MVLN, Rao SV, Radhika K, Chawak MM. Dietary supplementation of Spirulina and its effects on broiler chicken exposed to aflatoxicosis. Indian J Poult Sci. (2005) 40:36–40.

Google Scholar

97. Lokapirnasari WP, Yulianto AB, Legowo D, Agustono. The effect of Spirulina as feed additive to myocardial necrosis and leukocyte of chicken with avian influenza (H5N1) virus infection. Proc Chem. (2016) 18:213–7. doi: 10.1016/j.proche.2016.01.033

CrossRef Full Text | Google Scholar

98. Zeweil H, Abaza, IM, Zahran SM, Ahmed MH, Elaand HMA, Asmaa AS, et al. Effect of Spirulina platensisas dietary supplement on some biological traits for chickens under heat stress condition. Asian J Biomed Pharma Sci. (2016) 6:8–12.

Google Scholar

99. Shinde SR, Patil RA, Padghan PV. Effect of Spirulina supplementation on growth performance of broilers. J Pharm Phytochem. (2018) SP1:3265–7.

100. Sarker MS, Rafiq K, Rahman MM, Islam MS. Effects of Spirulina platensis on egg production and hematobiochemical parameters in layer birds. (MS Thesis), Department of Pharmacology, Bangladesh Agricultural University, Mymensingh, Bangladesh (2018).

101. Yang Y, Iji PA, Choct M. Dietary modulation of gut microflora in broiler chickens: a review of the role of six kinds of alternatives to in-feed antibiotics. World's Poult Sci J. (2009) 65:97–114. doi: 10.1017/S0043933909000087

PubMed Abstract | CrossRef Full Text | Google Scholar

102. Gaggia F, Mattarelli P, Biavati B. Probiotics and prebiotics in animal feeding for safe food production. Int J Food Microbiol. (2010) 141:S15–28. doi: 10.1016/j.ijfoodmicro.2010.02.031

PubMed Abstract | CrossRef Full Text | Google Scholar

103. Adil S, Magray SN. Impact and manipulation of gut microflora in poultry: a review. J Anim Vet Adv. (2012) 11:873–7. doi: 10.3923/javaa.2012.873.877

CrossRef Full Text | Google Scholar

104. Abdel-Raheem SM, Abd-Allah SMS, Hassanein KMA. The effects of prebiotic, probiotic and synbiotic supplementation on intestinal microbial ecology and histomorphology of broiler chickens. Int J Agro Vet Med Sci. (2012) 6:277–89. doi: 10.5455/ijavms.156

CrossRef Full Text | Google Scholar

105. Mookiah SS, Sieo CC, Ramasamy K, Abdullah N, Ho YW. Effects of dietary prebiotics, probiotic and symbiotic on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens. J Sci Food Agric. (2014) 94:341–8. doi: 10.1002/jsfa.6365

PubMed Abstract | CrossRef Full Text | Google Scholar

106. Awad W, Gharee K, Bohm J. Intestinal structure and function of broiler chickens on diets supplemented with a symbiotic containing enterococcus faecium and oligosaccharides. Int J Mol Sci. (2008) 9:2205–16. doi: 10.3390/ijms9112205

PubMed Abstract | CrossRef Full Text | Google Scholar

107. Hassanpour H, Moghaddam AKZ, Khosravi M, Mayahi M. Effects of synbiotic on the intestinal morphology and humoral immune response in broiler chickens. Livestock Sci. (2013) 153:116–22. doi: 10.1016/j.livsci.2013.02.004

PubMed Abstract | CrossRef Full Text | Google Scholar

108. Li X, Liu LQ, Xu C. Effects of supplementation of fructo-oligosaccharide and/or Bacillus subtilis to diets on performance and intestinal microflora in broilers. Archivfur Tierzucht. (2008) 51:64–70. doi: 10.5194/aab-51-64-2008

CrossRef Full Text | Google Scholar

109. Madej JP, Stefaniak T, Bednarczyk M. Effect of in ovo-delivered prebiotics and synbiotics on lymphoid-organs morphology in chickens. Poult Sci. (2015) 94:1209–19. doi: 10.3382/ps/pev076

PubMed Abstract | CrossRef Full Text | Google Scholar

110. Mokhtari R., Yazdani A, Kashfi H. The effects of different growth promoters on performance and carcass characteristics of broiler chickens. J Vet Med Anim Health. (2015) 7:271–7. doi: 10.5897/JVMAH2015.0394

PubMed Abstract | CrossRef Full Text | Google Scholar

111. Panda AK, Reddy MR, Ramarao SV, Raju M, Praharaj NK. Growth, carcass characteristics, immunocompetence and response to Escherichia coli of broilers fed diets with various levels of probiotic. Arch Für Geflügelkunde. (2000) 64:152–6.

Google Scholar

112. Yusrizal C, Chen TC. Effect of adding chicory fructans in feed on broiler growth performance, serum cholesterol, and intestinal length. Int J Poult Sci. (2003) 3:214–9. doi: 10.3923/ijps.2003.214.219

CrossRef Full Text | Google Scholar

113. Al-Sultan SI, Abdel-Raheem SM, El-Ghareeb WR, Mohamed MHA. Comparative effects of using prebiotic, probiotic, synbiotic and acidifier on growth performance, intestinal microbiology and histomorphology of broiler chicks. Jpn J Vet Res. (2016) 64:S187–95.

Google Scholar

114. Ren H, Vahjen W, Dadi T, Saliu EM, Boroojeni, Zentek J. Synergistic effects of probiotics and phytobiotics on the intestinal microbiota in young broiler chicken. Microorganisms. (2019) 7:684. doi: 10.3390/microorganisms7120684

PubMed Abstract | CrossRef Full Text | Google Scholar

115. Sapsuha Y, Suprijatna E, Kismitai S, Sugiharto S. Combination of probiotic and phytobiotic as an alternative for growth promoter for broilers chickens- a review. Livestock Res Rural Dev. (2021) 33. http://www.lrrd.org/lrrd33/4/3349yus_ar.html

Google Scholar

116. Denli, M, Okan F, Çelik K. Effect of dietary probiotic, organic acid and antibiotic supplementation to diets on broiler performance and carcass yield. Pak J Nutr. (2003) 2:89–91. doi: 10.3923/pjn.2003.89.91

CrossRef Full Text | Google Scholar

117. Wahyuni AETH, Prakasita VC, Nahak TEM, Tae AV, Ajiguna JC, Adrenalin SL, et al. The opportunities of feed additif of commercial herbal-probiotic “Promix®” feed as a substitute for antibiotic growth promoter (AGP) in broilers given ND vaccines. J Sain Vet. (2019) 37:180–4. doi: 10.22146/jsv.48614

CrossRef Full Text

118. Yuanita I, Sunarti D, Wahyuni HI, Suthama N. Feeding Dayak onion (Eleutherine palmifolia) extract and Lactobacillus acidophilus mixture on blood biochemicals, meat quality characteristics and growth performance in broiler chickens. Livestock Res Rural Dev. (2019) 31. http://www.lrrd.org/lrrd31/9/yuanit31144.html

Google Scholar

119. Chang CH, Teng PY, Lee TT, Yu B. Effects of multi-strain probiotics combined with Gardeniae fructus on intestinal microbiota, metabolites, and morphology in broilers. J Poult Sci. (2019) 56:32–43. doi: 10.2141/jpsa.0170179

PubMed Abstract | CrossRef Full Text | Google Scholar

120. Jung BG, Ko JH, Lee BJ. Dietary supplementation with a probiotic fermented four-herb combination enhances immune activity in broiler chicks and increases survivability against Salmonella gallinarum in experimentally infected broiler chicks. J Vet Med Sci. (2010) 72:1565–73. doi: 10.1292/jvms.10-0152

PubMed Abstract | CrossRef Full Text | Google Scholar

121. Hsu YM, Yu B, Tseng CS, Chang CH, Chen DS, Su CH, et al. Preventive activities of Scutellariae Radix, Gardeniae Fructus, and probiotics in Salmonella enterica serovar typhimurium infection in chickens. Anim Feed Sci Technol. (2016) 214:121–9. doi: 10.1016/j.anifeedsci.2016.02.004

CrossRef Full Text | Google Scholar

122. Prakasita VC, Asmara W, Widyarini S, Wahyuni AETH. Combination of herbs and probiotics as an alternative growth promoter: an in vitro study. Vet World. (2019) 12:614–20. doi: 10.14202/vetworld.2019.614-620

PubMed Abstract | CrossRef Full Text | Google Scholar

123. Risdianto D, Suthama N, Suprijatna E, Sunarso S. Inclusion effect of ginger and turmeric mixture combined with Lactobacillus spp. isolated from rumen fluid of cattle on health status and growth of broiler. J Indonesian Trop Anim Agric. (2019) 44:423–33. doi: 10.14710/jitaa.44.4.423-433

CrossRef Full Text | Google Scholar

124. Djezzar R, Benamirouche K, Ammi DB, Said RM, Guetarni D. Effect of a dietary supplementation combining a probiotic and a natural anticoccidial in broiler chickens. African J Agric Res. (2014) 9:3783–8.

Google Scholar

Keywords: growth promoters, probiotics, prebiotics, phytobiotics, spirulina, synbiotic, poultry

Citation: Rafiq K, Tofazzal Hossain M, Ahmed R, Hasan MM, Islam R, Hossen MI, Shaha SN and Islam MR (2022) Role of Different Growth Enhancers as Alternative to In-feed Antibiotics in Poultry Industry. Front. Vet. Sci. 8:794588. doi: 10.3389/fvets.2021.794588

Received: 13 October 2021; Accepted: 23 December 2021;
Published: 11 February 2022.

Edited by:

Einar Vargas-Bello-Pérez, University of Copenhagen, Denmark

Reviewed by:

Samuel N. Nahashon, Tennessee State University, United States
Aleksandra Dunislawska, University of Science and Technology (UTP), Poland

Copyright © 2022 Rafiq, Tofazzal Hossain, Ahmed, Hasan, Islam, Hossen, Shaha and Islam. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Kazi Rafiq, kazirafiq@bau.edu.bd

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