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RESEARCH ARTICLE

Dietary supplementation with avilamycin and Lactobacillus acidophilus effects growth performance and the expression of growth-related genes in broilers

A. A. Saleh https://orcid.org/0000-0002-2052-5248 A B , K. Amber A and A. A. Mohammed A
+ Author Affiliations
- Author Affiliations

A Department of Poultry Production, Faculty of Agriculture, Kafrelsheikh University, 333516 Kafrelsheikh, Egypt.

B Corresponding author. Email: ahmed.saleh1@agr.kfs.edu.eg

Animal Production Science 60(14) 1704-1710 https://doi.org/10.1071/AN19030
Submitted: 21 January 2019  Accepted: 24 February 2020   Published: 23 April 2020

Abstract

Context: The use of antibiotics in poultry production is appropriate; however, it brings a high risk of dissemination of antibiotic-resistant strains of pathogenic and non-pathogenic bacteria and their further transmission to humans via the food chain.

Aims: The effects of supplementation with Lactobacillus acidophilus (a probiotic) or avilamycin (an in-feed antibiotic growth promoter), on growth performance, digestibility, plasma lipid levels, and the expression of certain growth-related genes were investigated.

Methods: In total, 135 15-day-old broiler chicks were divided into three groups (n = 45): a control group and two treatment groups. Each treatment group was then further divided into three replicates (15 birds each). The control group was fed a basal diet; the second group received basal diet supplemented with avilamycin (0.1 g/kg); the third group received basal diet plus L. acidophilus (0.1 g/kg). Growth performance (bodyweight, feed intake and feed-conversion ratio) was measured. Digestibility and gene expression were measured at the end of the experiment.

Key results: Greatest bodyweight gain was achieved in the L. acidophilus-fed chicks, which were significantly (P < 0.05) heavier than the control chicks and the avilamycin-fed chicks. Addition of avilamycin or L. acidophilus to the diet also significantly improved feed efficiency (P < 0.05) compared with the control. Although the digestibility of dry matter, crude protein and crude fibre significantly improved in the two experimental groups compared with the control, ether extract was not affected. In addition, plasma total cholesterol, triglyceride and low-density-lipoprotein cholesterol levels were significantly (P < 0.05) decreased whereas plasma high-density-lipoprotein cholesterol was significantly (P < 0.05) increased in the L. acidophilus group compared with the control. Expression of the genes for growth hormone secretagogue receptor (GHSR), insulin-like growth factor 1 (IGF-1) and insulin-like growth factor 1 receptor (IGF1R) was remarkably upregulated in the skeletal muscles of the two experimental groups.

Conclusions: Supplementation with L. acidophilus (0.1 g/kg) in the broiler diet had positive effects on growth, feed intake, feed efficiency, digestibility, and plasma lipid levels of the broilers.

Implications: Lactobacillus acidophilus might be a more useful additive in broiler feed than antibiotic growth promoters such as avilamycin.

Additional keywords: biochemistry, digestion, nutrition, probiotics, RNA.


References

Abd El-Moneim EA, El-Wardany I, Abu-Taleb AM, Wakwak MM, Ebeid TA, Saleh AA (2019a) Assessment of on ovo administration of Bifidobacterium bifidum and Bifidobacterium longum on performance, ileal histomorphometry, blood hematological, and biochemical parameters of broilers. Probiotics and Antimicrobial Proteins.
Assessment of on ovo administration of Bifidobacterium bifidum and Bifidobacterium longum on performance, ileal histomorphometry, blood hematological, and biochemical parameters of broilers.Crossref | GoogleScholarGoogle Scholar |

Abdel-Moneim EA, Dina AS, Hamdy AB, Essam MS, Saleh AA, Ebeid TA (2019b) Effect of dietary supplementation of Bacillus subtilis spores on growth performance, oxidative status, and digestive enzyme activities in Japanese quail birds. Tropical Animal Health and Production 52, 671–680.
Effect of dietary supplementation of Bacillus subtilis spores on growth performance, oxidative status, and digestive enzyme activities in Japanese quail birds.Crossref | GoogleScholarGoogle Scholar |

Abdulrahim SM, Haddadin MSY, Hashlamoun EAR, Robinson RK (1993) The influence of Lactobacillus acidophilus and bacitracin on layer performance of chickens and cholesterol content of plasma and egg yolk. British Poultry Science 3, 341–346.

Beccavin C, Chevalier B, Duclos MJ (1999) Circulating insulin-like growth factors (IGF-I and -II) and IGF binding proteins in divergently selected fat or lean chickens: effect of prolonged fasting. Growth Hormone and IGF Research 9, 187–194.
Circulating insulin-like growth factors (IGF-I and -II) and IGF binding proteins in divergently selected fat or lean chickens: effect of prolonged fasting.Crossref | GoogleScholarGoogle Scholar | 10502455PubMed |

Beccavin C, Chevalier B, Duclos MJ (2001) Insulin-like growth factors and body growth in chickens divergently selected for high or low growth rate. The Journal of Endocrinology 168, 297–306.
Insulin-like growth factors and body growth in chickens divergently selected for high or low growth rate.Crossref | GoogleScholarGoogle Scholar | 11182767PubMed |

Buck LM, Gilliand SE (1994) Comparisons of freshly isolated strains of Lactobacillus acidophilus of human intestinal origin for ability to assimilate cholesterol during growth. Journal of Dairy Science 77, 2925–2933.
Comparisons of freshly isolated strains of Lactobacillus acidophilus of human intestinal origin for ability to assimilate cholesterol during growth.Crossref | GoogleScholarGoogle Scholar | 7836579PubMed |

Chi MS, Koh ET, Stewart TJ (1982) Effects of garlic on lipid metabolism in rats fed cholesterol or lard. The Journal of Nutrition 112, 241–248.
Effects of garlic on lipid metabolism in rats fed cholesterol or lard.Crossref | GoogleScholarGoogle Scholar | 7057262PubMed |

Choi K, Lehman DW, Law JM (2007) Hypoxia-reperfusion triggers immunocompromise in Nile tilapia (Oreochromis niloticus). Journal of Aquatic Animal Health 19, 128–140.
Hypoxia-reperfusion triggers immunocompromise in Nile tilapia (Oreochromis niloticus).Crossref | GoogleScholarGoogle Scholar | 18201054PubMed |

Davis GS, Anderson KE (2002) The effects of feeding the direct-fed microbial, primalac, on growth parameters and egg production in single comb white leghorn hens. Poultry Science 81, 755–759.
The effects of feeding the direct-fed microbial, primalac, on growth parameters and egg production in single comb white leghorn hens.Crossref | GoogleScholarGoogle Scholar | 12079039PubMed |

Delzenne NM, Kok N, Roberfroid MB (1993) Dietary fructooligosaccharides modify lipid metabolism in rats. The American Journal of Clinical Nutrition 57, 820S
Dietary fructooligosaccharides modify lipid metabolism in rats.Crossref | GoogleScholarGoogle Scholar |

Denli M, Okan F, Celik K (2003) Effect of dietary probiotic, organic acid and antibiotic supplementation to diets on broiler performance and carcass yield. Pakistan Journal of Nutrition 2, 89–91.
Effect of dietary probiotic, organic acid and antibiotic supplementation to diets on broiler performance and carcass yield.Crossref | GoogleScholarGoogle Scholar |

Ding W, Wang H, Griffiths MW (2005) Probiotics down-regulate flaA σ28 promoter in Campylobacter jejuni. Journal of Food Protection 68, 2295–2300.
Probiotics down-regulate flaA σ28 promoter in Campylobacter jejuni.Crossref | GoogleScholarGoogle Scholar | 16300065PubMed |

Duclos M, Beccavin C, Simon J (1999) Genetic models for the study of insulin-like growth factors (IGF) and muscle development in birds compared to mammals. Domestic Animal Endocrinology 17, 231–243.
Genetic models for the study of insulin-like growth factors (IGF) and muscle development in birds compared to mammals.Crossref | GoogleScholarGoogle Scholar | 10527126PubMed |

Emadi M, Kermanshahi H (2006) Effect of turmeric rhizome powder on performance and carcass characteristics of broiler chickens. International Journal of Poultry Science 5, 1069–1072.
Effect of turmeric rhizome powder on performance and carcass characteristics of broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Farhat A, Chavez ER (1999) Effects of line, dietary protein, sex, age, and feed withdrawal on insulin-like growth factor-I in White Pekin ducks. Poultry Science 78, 1307–1312.
Effects of line, dietary protein, sex, age, and feed withdrawal on insulin-like growth factor-I in White Pekin ducks.Crossref | GoogleScholarGoogle Scholar | 10515362PubMed |

Florini JR, Ewton DZ, Magri KA (1991) Hormones, growth factors, and myogenic differentiation. Annual Review of Physiology 53, 201–216.
Hormones, growth factors, and myogenic differentiation.Crossref | GoogleScholarGoogle Scholar | 2042960PubMed |

Gaskins HR, Collier CT, Anderson DB (2002) Antibiotics as growth promotants: mode of action. Animal Biotechnology 13, 29–42.
Antibiotics as growth promotants: mode of action.Crossref | GoogleScholarGoogle Scholar | 12212942PubMed |

Gilliland SE, Nelson CR, Maxwell C (1985) Assimilation of cholesterol by Lactobacillus acidophilus. Applied and Environmental Microbiology 49, 377–381.
Assimilation of cholesterol by Lactobacillus acidophilus.Crossref | GoogleScholarGoogle Scholar | 3920964PubMed |

Grunewald KK (1982) Serum cholesterol levels in rats fed skim milk fermented by Lactobacillus acidophilus. Journal of Food Science 47, 2078–2079.
Serum cholesterol levels in rats fed skim milk fermented by Lactobacillus acidophilus.Crossref | GoogleScholarGoogle Scholar |

Gunal M, Yayli G, Kaya O, Karahan N, Sulak O (2006) The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. International Journal of Poultry Science 5, 149–155.
The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers.Crossref | GoogleScholarGoogle Scholar |

Guobin C, Xiangping L, Jing L (2011) Temporal and spatial expression of the Pax-7 gene during chicken embryo and postnatal development. Journal of Animal and Veterinary Advances 10, 1785–1788.
Temporal and spatial expression of the Pax-7 gene during chicken embryo and postnatal development.Crossref | GoogleScholarGoogle Scholar |

Harrison VC, Peat G (1975) Serum cholesterol and bowel flora in the newborn. The American Journal of Clinical Nutrition 28, 1351–1355.
Serum cholesterol and bowel flora in the newborn.Crossref | GoogleScholarGoogle Scholar |

Jamroz D, Kirchgessner M, Wiliczkiewicz JO (1995) Effect of application of avilamycin (Maxus) and different levels of crude protein in concentrate mixtures on the nitrogen excretion and retention and on the apparent digestibility of amino acids in broiler chickens. Archiv für Geflügelkunde 59, 152–157.

Jin LZ, Ho YW, Ali AM, Abdullah N, Jalaludin S (1996a) Influence of dried Bacillus subtilis and lactobacilli cultures on intestinal microflora and performance in broilers. Asian–Australasian Journal of Animal Sciences 9, 397–404.
Influence of dried Bacillus subtilis and lactobacilli cultures on intestinal microflora and performance in broilers.Crossref | GoogleScholarGoogle Scholar |

Jin LZ, Ho YW, Ali AM, Abdullah N, Jalaludin S (1996b) Antagonistic effects of intestinal Lactobacillus isolates on pathogens of chicken. Letters in Applied Microbiology 23, 67–71.
Antagonistic effects of intestinal Lactobacillus isolates on pathogens of chicken.Crossref | GoogleScholarGoogle Scholar | 8987444PubMed |

Jin LZ, Ho YW, Ali AM, Abdullah N, Jalaludin S (1996c) Effect of adherent Lactobacillus spp. on in vitro adherence of salmonellae to the intestinal epithelial cells of chickens. The Journal of Applied Bacteriology 81, 201–206.
Effect of adherent Lactobacillus spp. on in vitro adherence of salmonellae to the intestinal epithelial cells of chickens.Crossref | GoogleScholarGoogle Scholar | 8760330PubMed |

Jin LZ, Ho YW, Ali AM, Abdullah N, Jalaludin S (1996d) Adhesion of Lactobacillus isolates to intestinal epithelial cells of chicken. Letters in Applied Microbiology 22, 229–232.
Adhesion of Lactobacillus isolates to intestinal epithelial cells of chicken.Crossref | GoogleScholarGoogle Scholar | 8852352PubMed |

Jin LZ, Ho YW, Ali AM, Abdullah N, Jalaludin S (1998) Growth performance, intestinal microbial populations and serum cholesterol of broilers fed diet containing Lactobacillus cultures. Poultry Science 77, 1259–1265.
Growth performance, intestinal microbial populations and serum cholesterol of broilers fed diet containing Lactobacillus cultures.Crossref | GoogleScholarGoogle Scholar | 9733111PubMed |

Jones FT, Ricket SC (2003) Observations on the history of the development of antimicrobials and their use in poultry feeds. Poultry Science 82, 613–617.
Observations on the history of the development of antimicrobials and their use in poultry feeds.Crossref | GoogleScholarGoogle Scholar | 12710481PubMed |

Kim M, Shin HK (1998) The water soluble extract of chicory influences serum and liver lipid concentrations, cecal short-chain fatty acid concentrations and fecal lipid excretion in rats. The Journal of Nutrition 128, 1731–1736.
The water soluble extract of chicory influences serum and liver lipid concentrations, cecal short-chain fatty acid concentrations and fecal lipid excretion in rats.Crossref | GoogleScholarGoogle Scholar | 9772143PubMed |

Klaver FAM, Van-der-Meer R (1993) The assumed assimilation of cholesterol by lactobacilli and Bifidobacterium bifidum is due to their bile salt deconjugating activity. Applied and Environmental Microbiology 59, 1120–1124.
The assumed assimilation of cholesterol by lactobacilli and Bifidobacterium bifidum is due to their bile salt deconjugating activity.Crossref | GoogleScholarGoogle Scholar |

Miles RD, Butcher GD, Henry PR, Littell RC (2006) Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology. Poultry Science 85, 476–485.
Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology.Crossref | GoogleScholarGoogle Scholar | 16553279PubMed |

Mohan B, Kadirvel R, Natarajan A, Bhaskaran M (1996) Effect of probiotic supplementation on growth, nitrogen utilisation and serum cholesterol in broilers. British Poultry Science 37, 395–401.
Effect of probiotic supplementation on growth, nitrogen utilisation and serum cholesterol in broilers.Crossref | GoogleScholarGoogle Scholar | 8773848PubMed |

Nava GM, Bielke LR, Callaway TR, Castaneda MP (2005) Probiotic alternatives to reduce gastrointestinal infections: the poultry experience. Animal Health Research Reviews 6, 105–118.
Probiotic alternatives to reduce gastrointestinal infections: the poultry experience.Crossref | GoogleScholarGoogle Scholar | 16164012PubMed |

Navidshad B, Adibmoradi M, Ansari Z (2010) Effect of Aspergillus meal prebiotic (Fermacto) on performance and intestinal morphology of broiler chickens fed diluted diets. Italian Journal of Animal Science 9, e55–e60.
Effect of Aspergillus meal prebiotic (Fermacto) on performance and intestinal morphology of broiler chickens fed diluted diets.Crossref | GoogleScholarGoogle Scholar |

Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR (2012) Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One 7, e43928
Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry.Crossref | GoogleScholarGoogle Scholar | 22962594PubMed |

NRC (1994) ‘Nutrient requirements of poultry, 9th edn.’ (National Academy Press: Washington, DC)

Pfaller MA (2006) Flavophospholipol use in animals: positive implications for antimicrobial resistance based on its microbiologic properties. Diagnostic Microbiology and Infectious Disease 56, 115–121.
Flavophospholipol use in animals: positive implications for antimicrobial resistance based on its microbiologic properties.Crossref | GoogleScholarGoogle Scholar | 16698216PubMed |

Qureshi AA, Crenshaw TD, Abuiremeileh N, Peterson DM, Elson CE (1987) Influence of minor plant constituents on porcine hepatic lipid metabolism: impact on serum lipid. Atherosclerosis 64, 109–115.
Influence of minor plant constituents on porcine hepatic lipid metabolism: impact on serum lipid.Crossref | GoogleScholarGoogle Scholar | 3606707PubMed |

Reid G, Sanders ME, Gaskins HR, Gibson GR, Mercenier A (2003) New scientific paradigms for probiotics and prebiotics. Journal of Clinical Gastroenterology 37, 105–118.
New scientific paradigms for probiotics and prebiotics.Crossref | GoogleScholarGoogle Scholar | 12869879PubMed |

Saleh AA (2014) Nigella seed oil as alternative to avilamycin antibiotic in broiler chicken diets. South African Journal of Animal Science 44, 254–261.
Nigella seed oil as alternative to avilamycin antibiotic in broiler chicken diets.Crossref | GoogleScholarGoogle Scholar |

Saleh AA, Ohtsuka A, Hayashi K (2011) Effects of feeding Aspergillus awamori and Aspergillus niger on growth performance and meat quality in broiler chickens. Journal of Poultry Science 48, 201–206.
Effects of feeding Aspergillus awamori and Aspergillus niger on growth performance and meat quality in broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Saleh AA, Ohtsuka A, Hayashi K (2012) Feeding Aspergillus awamori reduces skeletal muscle protein breakdown and stimulates growth in broilers. Animal Science Journal 83, 594–598.
Feeding Aspergillus awamori reduces skeletal muscle protein breakdown and stimulates growth in broilers.Crossref | GoogleScholarGoogle Scholar | 22862929PubMed |

Saleh AA, Hayashi K, Ohtsuka A (2013) Synergistic effect of feeding Aspergillus awamori and Saccharomyces cerevisiae on growth performance in broiler chickens; promotion of protein metabolism and modification of fatty acid profile in the muscle. Journal of Poultry Science 50, 242–250.
Synergistic effect of feeding Aspergillus awamori and Saccharomyces cerevisiae on growth performance in broiler chickens; promotion of protein metabolism and modification of fatty acid profile in the muscle.Crossref | GoogleScholarGoogle Scholar |

Saleh AA, Gálik B, Arpášová H, Capcarová M, Kalafová A, Šimko M, Juráček M, Rolinec M, Bíro D, Abudabos AM (2017) Synergistic effect of feeding Aspergillus awamori and lactic acid bacteria on performance, egg traits, egg yolk cholesterol and fatty acid profile in laying hens. Italian Journal of Animal Science 16, 132–139.
Synergistic effect of feeding Aspergillus awamori and lactic acid bacteria on performance, egg traits, egg yolk cholesterol and fatty acid profile in laying hens.Crossref | GoogleScholarGoogle Scholar |

Saleh AA, Ebeid TA, Abudabos AM (2018a) Effect of dietary phytogenics (herbal mixture) supplementation on growth performance, nutrient utilization, antioxidative properties, and immune response in broilers. Environmental Science and Pollution Research International 25, 14606–14613.
Effect of dietary phytogenics (herbal mixture) supplementation on growth performance, nutrient utilization, antioxidative properties, and immune response in broilers.Crossref | GoogleScholarGoogle Scholar | 29532373PubMed |

Saleh AA, El-Far AH, Abdel-Latif MA, Emam MA, Ghanem R, Abd El-Hamid HS (2018b) Exogenous dietary enzyme formulations improve growth performance of broiler chickens fed a low-energy diet targeting the intestinal nutrient transporter genes. PLoS One 13, e0198085
Exogenous dietary enzyme formulations improve growth performance of broiler chickens fed a low-energy diet targeting the intestinal nutrient transporter genes.Crossref | GoogleScholarGoogle Scholar | 29847558PubMed |

Schwarz S, Kehrenberg C, Walsh TR (2001) Use of antimicrobial agents in veterinary medicine and food animal production. International Journal of Antimicrobial Agents 17, 431–437.
Use of antimicrobial agents in veterinary medicine and food animal production.Crossref | GoogleScholarGoogle Scholar | 11397611PubMed |

Stewart C, Rotwein P (1996) Growth differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiological Reviews 76, 1005–1026.
Growth differentiation, and survival: multiple physiological functions for insulin-like growth factors.Crossref | GoogleScholarGoogle Scholar | 8874492PubMed |

Sun Y, Wang P, Smith RG (2004) Ghrelin stimulation of growth hormone release and appetite is mediated through the growth hormone secretagogue receptor. Proceedings of the National Academy of Sciences 101, 4679–4684.
Ghrelin stimulation of growth hormone release and appetite is mediated through the growth hormone secretagogue receptor.Crossref | GoogleScholarGoogle Scholar |

Talebi A, Amirzadeh B, Mokhtari B, Gahri H (2008) Effects of a multi-strain probiotic (PrimaLac) on performance and antibody responses to Newcastle disease virus and infectious bursal disease virus vaccination in broiler chickens. Avian Pathology 37, 509–512.
Effects of a multi-strain probiotic (PrimaLac) on performance and antibody responses to Newcastle disease virus and infectious bursal disease virus vaccination in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 18798026PubMed |

Valadirova L, Sourdjiisda S, Dilow T (1997) Nutritive effect of avilamycin supplementation to chicken broiler mixes. Zhivotnov’Dni-Nauki 34, 49–52.

Waldroup A, Kaniawato S, Mauromoustakos A (1995) Performance characteristics and microbiological aspects of broiler fed diets supplemented with organic acids. Journal of Food Protection 58, 482–489.
Performance characteristics and microbiological aspects of broiler fed diets supplemented with organic acids.Crossref | GoogleScholarGoogle Scholar | 31137267PubMed |

Wellenreiter RH Mowrey DH Stobbs LA d'Assonville JA 2000 Effects of avilamycin on performance of broiler chickens. Veterinary Therapeutics 1 118 124

Xu ZR, Hu C, Wang MQ (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82, 1030–1036.
Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers.Crossref | GoogleScholarGoogle Scholar | 12817461PubMed |

Yamamoto M, Saleh F, Ohtsuka A (2005) New fermentation technique to process fish waste. Animal Science Journal 76, 245–248.
New fermentation technique to process fish waste.Crossref | GoogleScholarGoogle Scholar |

Yeo J, Kim K (1997) Effect of feeding diets containing an antibiotic, a probiotic, or yucca extract on growth and intestinal urease activity in broiler chicks. Poultry Science 76, 381–385.
Effect of feeding diets containing an antibiotic, a probiotic, or yucca extract on growth and intestinal urease activity in broiler chicks.Crossref | GoogleScholarGoogle Scholar | 9057222PubMed |

Zhan C (1998) The action of decreasing cholesterol of Bifidobacterium: precipitation and assimilation with biliary salt. Medicine in Abroad: Antibiotic 19, 146–149.

Zigman JM, Nakano Y, Elmquist JK (2005) Mice lacking ghrelin receptors resist the development of diet-induced obesity. The Journal of Clinical Investigation 115, 3564–3572.
Mice lacking ghrelin receptors resist the development of diet-induced obesity.Crossref | GoogleScholarGoogle Scholar | 16322794PubMed |