Skip to main content
Log in

Impact of multi-strain probiotic, citric acid, garlic powder or their combinations on performance, ileal histomorphometry, microbial enumeration and humoral immunity of broiler chickens

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Heat stress, one of the critical obstacles to poultry sector in subtropical and tropical countries, reduces performance, immune response, and animal welfare. This study examined the effect of dietary inclusion of probiotic (PRO), citric acid (CIT), garlic powder (GAR) or their combinations on growth, blood constituents, ileal microflora and morphology and humoral immunity of broiler chickens subjected to cyclic heat stress. Four hundred ninety one-day-old Ross-308 broiler chicks were randomly allocated to 7 groups with 7 replicates of 10 birds each as follows: control (C) group received the basal diet without supplements, PRO, CIT and GAR groups supplemented with 0.5 g kg−1 multi-strain probiotic mixture (MPM), citric acid and garlic powder, respectively. PRO-CIT and PRO-GAR groups treated with 0.5 g kg−1 MPM, and 0.5 g kg−1 citric acid and garlic powder, while CIT-GAR group fed diet with 0.5 g kg−1 of citric acid and garlic powder. Results revealed that dietary supplements and their combinations improved (P < 0.001) growth performance and decreased abdominal fat of heat-stressed birds. Dietary supplements decreased (P < 0.01) serum concentrations of cholesterol, triglycerides and LDL, while HDL was elevated (P < 0.05). Feed additives reduced (P < 0.01) ileal enumeration of Escherichia coli and total coliform while Lactobacillus count was increased (P < 0.05) only in MPM-enriched groups. Supplementation of these natural products improved (P < 0.01) ileal architecture while humoral immune response was not significantly influenced except antibody titre against Newcastle disease virus which was increased (P < 0.05) in MPM-supplemented groups. Conclusively, addition of the dietary supplements and their combinations, particularly, probiotic and citric acid combination can improve productive performance, and intestinal flora and histomorphometry of broilers exposed to cyclic heat stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abd El-Hack, M.E., Abdelnour, S.A., Abd El-Moneim, A.E., Arif, M., Khafaga, A., Shaheen, H., Samak, D. and Swelum, A.A., 2019. Putative impacts of phytogenic additives to ameliorate lead toxicity in animal feed, Environmental Science and Pollution Research, 26, 23209–23218

    Article  CAS  PubMed  Google Scholar 

  • Abd El-Hack, M.E., Alagawany, M., Abdel-Moneim, A.-M.E., Mohammed, N.G., Khafaga, A.F., Bin-Jumah, M., Othman, S.I., Allam, A.A. and Elnesr, S.S., 2020a. Cinnamon (Cinnamomum zeylanicum) Oil as a Potential Alternative to Antibiotics in Poultry, Antibiotics, 9, 210-221

    Article  CAS  PubMed Central  Google Scholar 

  • Abd El-Hack, M.E., El-Saadony, M.T., Shafi, M.E., Qattan, S.Y., Batiha, G.E., Khafaga, A.F., Abdel-Moneim, A.M.E. and Alagawany, M., 2020b. Probiotics in poultry feed: A comprehensive review, Journal of animal physiology and animal nutrition, 104, 1835–1850

    Article  CAS  PubMed  Google Scholar 

  • Abd El-Moneim, A.E. and Sabic, E.M., 2019. Beneficial effect of feeding olive pulp and Aspergillus awamori on productive performance, egg quality, serum/yolk cholesterol and oxidative status in laying Japanese quails, Journal of Animal and Feed Sciences, 28, 52-61

    Article  Google Scholar 

  • Abd El-Moneim, A.E., Sabic, E.M. and Abu-Taleb, A.M., 2019. Influence of dietary supplementation of irradiated or non-irradiated olive pulp on biochemical profile, antioxidant status and immune response of Japanese quails, Biological Rhythm Research, In Press

  • Abd El-Moneim, E.A., El-Wardany, I., Abu-Taleb, A.M., Wakwak, M.M., Ebeid, T.A. and Saleh, A.A., 2020. Assessment of in ovo administration of Bifidobacterium bifidum and Bifidobacterium longum on performance, ileal histomorphometry, blood hematological, and biochemical parameters of broilers, Probiotics and Antimicrobial Proteins, 12, 439-450

    Article  PubMed  Google Scholar 

  • Abdel-Moneim, A.-M.E., Sabic, E., Abu-Taleb, A. and Ibrahim, N., 2020a. Growth performance, hemato-biochemical indices, thyroid activity, antioxidant status, and immune response of growing Japanese quail fed diet with full-fat canola seeds, Tropical Animal Health and Production, 52, 1853–1862

    Article  PubMed  Google Scholar 

  • Abdel-Moneim, A.-M.E., Selim, D.A., Basuony, H.A., Sabic, E.M., Saleh, A.A. and Ebeid, T.A., 2020b. 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

    Article  PubMed  Google Scholar 

  • Abdel-Moneim, A.E., Elbaz, A.M., Khidr, R.E. and Badri, F.B., 2020c. Effect of in ovo inoculation of Bifidobacterium spp. on growth performance, thyroid activity, ileum histomorphometry and microbial enumeration of broilers, Probiotics and Antimicrobial Proteins, 12, 873–882

    Article  CAS  PubMed  Google Scholar 

  • Abo Ghanima, M.M., Bin-Jumah, M., Abdel-Moneim, A.-M.E., Khafaga, A.F., Abd El-Hack, M.E., Allam, A.A. and El-Kasrawy, N.I., 2020. Impacts of Strain Variation on Response to Heat Stress and Boldo Extract Supplementation to Broiler Chickens, Animals, 10, 24

    Article  Google Scholar 

  • Abou-Kassem, D. et al., 2021. Growth, carcass characteristics, meat quality and microbial aspects of growing quail fed diets enriched with two different types of probiotics (Bacillus toyonensis and Bifidobacterium bifidum), Poultry science, 100, 84-93

    Article  CAS  PubMed  Google Scholar 

  • Abudabos, A., Alyemni, A., Dafalla, Y. and Khan, R., 2017. Effect of organic acid blend and bacillus subtilis alone or in combination on growth traits, blood biochemical and antioxidant status in broilers exposed to salmonella typhimurium challenge during the starter phase, Journal of Applied Animal Research, 45, 538–542

    Article  CAS  Google Scholar 

  • Adil, S., Banday, T., Bhat, G., Mir, M. and Rehman, M., 2010. Effect of dietary supplementation of organic acids on performance, intestinal histomorphology, and serum biochemistry of broiler chicken, Veterinary medicine international, 2010,

    Google Scholar 

  • Agboola, A., Omidiwura, B., Odu, O., Popoola, I. and Iyayi, E., 2015. Effects of organic acid and probiotic on performance and gut morphology in broiler chickens, South African Journal of Animal Science, 45, 494-501

    Article  CAS  Google Scholar 

  • Al-Fataftah, A.-R. and Abdelqader, A., 2014. Effects of dietary Bacillus subtilis on heat-stressed broilers performance, intestinal morphology and microflora composition, Animal Feed Science and Technology, 198, 279-285

    Article  CAS  Google Scholar 

  • Allahdo, P., Ghodraty, J., Zarghi, H., Saadatfar, Z., Kermanshahi, H. and Dovom, M., 2018. Effect of probiotic and vinegar ongrowth performance, meat yields, immune responses, and small intestine morphology of broilerchickens, Italian Journal of Animal Science, 17, 675-685

    Article  CAS  Google Scholar 

  • Ao, T., Cantor, A., Pescatore, A., Ford, M., Pierce, J. and Dawson, K., 2009. Effect of enzyme supplementation and acidification of diets on nutrient digestibility and growth performance of broiler chicks, Poultry science, 88, 111–117

    Article  CAS  PubMed  Google Scholar 

  • Attia, Y., Al-Harthi, M., El-Shafey, A., Rehab, Y. and Kim, W., 2017. Enhancing tolerance of broiler chickens to heat stress by supplementation with vitamin E, vitamin C and/or probiotics, Annals of Animal Science, 17, 1155–1169

    Article  CAS  Google Scholar 

  • Baurhoo, B., Ferket, P. and Zhao, X., 2009. Effects of diets containing different concentrations of mannanoligosaccharide or antibiotics on growth performance, intestinal development, cecal and litter microbial populations, and carcass parameters of broilers, Poultry science, 88, 2262-2272

    Article  CAS  PubMed  Google Scholar 

  • Czerwiński, J., Højberg, O., Smulikowska, S., Engberg, R.M. and Mieczkowska, A., 2012. Effects of sodium butyrate and salinomycin upon intestinal microbiota, mucosal morphology and performance of broiler chickens, Archives of animal nutrition, 66, 102-116

    Article  PubMed  Google Scholar 

  • Dehghani-Tafti, N. and Jahanian, R., 2016. Effect of supplemental organic acids on performance, carcass characteristics, and serum biochemical metabolites in broilers fed diets containing different crude protein levels, Animal Feed Science and Technology, 211, 109-116

    Article  CAS  Google Scholar 

  • Dela Cruz, P.J.D., Dagaas, C.T., Mangubat, K.M.M., Angeles, A.A. and Abanto, O.D., 2019. Dietary effects of commercial probiotics on growth performance, digestibility, and intestinal morphometry of broiler chickens, Tropical Animal Health and Production, 51, 1105-1115

    Article  Google Scholar 

  • Diarra, S.S. and Tabuaciri, P., 2014. Feeding management of poultry in high environmental temperatures, International Journal of Poultry Science, 13, 657-661

    Article  Google Scholar 

  • Dibner, J. and Buttin, P., 2002. Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism, Journal of applied poultry research, 11, 453-463

    Article  CAS  Google Scholar 

  • Ebeid, T., Fathi, M., Al-Homidan, I., Ibrahim, Z. and Al-Sagan, A., 2019. Effect of dietary probiotics and stocking density on carcass traits, meat quality, microbial populations and ileal histomorphology in broilers under hot-climate conditions, Animal Production Science, 59, 1711–1719

    Article  Google Scholar 

  • Farnell, M., Donoghue, A., De Los Santos, F.S., Blore, P., Hargis, B., Tellez, G. and Donoghue, D., 2006. Upregulation of oxidative burst and degranulation in chicken heterophils stimulated with probiotic bacteria, Poultry science, 85, 1900-1906

    Article  CAS  PubMed  Google Scholar 

  • Gadde, U., Kim, W., Oh, S. and Lillehoj, H.S., 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review, Animal health research reviews, 18, 26-45

    Article  CAS  PubMed  Google Scholar 

  • Hamed, D.M. and Hassan, A.M.A., 2013. Acids supplementation to drinking water and their effects on Japanese quails experimentally challenged with Salmonella Enteritidis, Research in Zoology, 3, 15-22

    Google Scholar 

  • Ibrahim, N., Sabic, E., Abu-Taleb, A. and Abdel-Moneim, A., 2020. Effect of dietary supplementation of full-fat canola seeds on productive performance, blood metabolites and antioxidant status of laying Japanese quails, Brazilian Journal of Poultry Science, 22, 1-10

    Article  Google Scholar 

  • Karangiya, V., Savsani, H., Patil, S.S., Garg, D., Murthy, K., Ribadiya, N. and Vekariya, S., 2016. Effect of dietary supplementation of garlic, ginger and their combination on feed intake, growth performance and economics in commercial broilers, Veterinary world, 9, 245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan, S.H. and Iqbal, J., 2016. Recent advances in the role of organic acids in poultry nutrition, Journal of Applied Animal Research, 44, 359-369

    Article  CAS  Google Scholar 

  • Kim, H.-Y., Eo, E.-Y., Park, H., Kim, Y.-C., Park, S., Shin, H.-J. and Kim, K., 2010. Medicinal herbal extracts of Sophorae radix, Acanthopanacis cortex, Sanguisorbae radix and Torilis fructus inhibit coronavirus replication in vitro, Antivir Ther, 15, 697-709

    CAS  PubMed  Google Scholar 

  • Maynard, C.L., Elson, C.O., Hatton, R.D. and Weaver, C.T., 2012. Reciprocal interactions of the intestinal microbiota and immune system, Nature, 489, 231-241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukherjee, A., Banerjee, G., Mukherjee, P., Ray, A.K., Chandra, G. and Ghosh, K., 2019. Antibacterial substances produced by pathogen inhibitory gut bacteria in Labeo rohita: Physico-chemical characterization, purification and identification through MALDI-TOF mass spectrometry, Microbial pathogenesis, 130, 146-155

    Article  CAS  PubMed  Google Scholar 

  • Nandi, A., Banerjee, G., Dan, S.K., Ghosh, K. and Ray, A.K., 2017. Probiotic efficiency of Bacillus sp. in Labeo rohita challenged by Aeromonas hydrophila: assessment of stress profile, haemato-biochemical parameters and immune responses, Aquaculture Research, 48, 4334-4345

    Article  CAS  Google Scholar 

  • NRC, 1994. Nutrition Requirements of Poultry, (National Academy Press, Washington, DC)

    Google Scholar 

  • Onibi, G., Adebisi, O., Fajemisin, A. and Adetunji, A., 2009. Response of broiler chickens in terms of performance and meat quality to garlic (Allium sativum) supplementation, African Journal of Agricultural Research, 4, 511-517

    Google Scholar 

  • Palamidi, I., Fegeros, K., Mohnl, M., Abdelrahman, W., Schatzmayr, G., Theodoropoulos, G. and Mountzouris, K., 2016. Probiotic form effects on growth performance, digestive function, and immune related biomarkers in broilers, Poultry science, 95, 1598-1608

    Article  CAS  PubMed  Google Scholar 

  • Pender, C.M., Kim, S., Potter, T.D., Ritzi, M.M., Young, M. and Dalloul, R.A., 2017. In ovo supplementation of probiotics and its effects on performance and immune-related gene expression in broiler chicks, Poultry science, 96, 1052-1062

    Article  CAS  PubMed  Google Scholar 

  • Pourakbari, M., Seidavi, A., Asadpour, L. and Martínez, A., 2016. Probiotic level effects on growth performance, carcass traits, blood parameters, cecal microbiota, and immune response of broilers, Anais da Academia Brasileira de Ciências, 88, 1011-1021

    Article  CAS  PubMed  Google Scholar 

  • Prasad, R., Rose, M., Vermani, M., Garg, S. and Puri, J., 2009. Lipid profile of chicken (Gallus domesticus) in response to dietary supplementation of garlic (Allium sativum), International Journal of Poultry Science, 8, 270-276

    Article  CAS  Google Scholar 

  • Ricke, S., 2003. The gastrointestinal tract ecology of Salmonella Enteritidis colonization in molting hens, Poultry science, 82, 1003-1007

    Article  CAS  PubMed  Google Scholar 

  • Rivlin, R.S., 2001. Historical perspective on the use of garlic, The Journal of Nutrition, 131, 951S-954S

    Article  CAS  PubMed  Google Scholar 

  • Sabour, S., Tabeidian, S.A. and Sadeghi, G., 2019. Dietary organic acid and fiber sources affect performance, intestinal morphology, immune responses and gut microflora in broilers, Animal Nutrition, 5, 156-162

    Article  PubMed  Google Scholar 

  • Saleh, A.A. et al., 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

    Article  CAS  Google Scholar 

  • Saleh, A.A., Eltantawy, M.S., Gawish, E.M., Younis, H.H., Amber, K.A., Abd El-Moneim, A.E.-M.E. and Ebeid, T.A., 2019. Impact of Dietary Organic Mineral Supplementation on Reproductive Performance, Egg Quality Characteristics, Lipid Oxidation, Ovarian Follicular Development, and Immune Response in Laying Hens Under High Ambient Temperature, Biological trace element research, 195, 506–514

    Article  PubMed  Google Scholar 

  • Salehizadeh, M., Modarressi, M.H., Mousavi, S.N. and Ebrahimi, M.T., 2019. Effects of probiotic lactic acid bacteria on growth performance, carcass characteristics, hematological indices, humoral immunity, and IGF-I gene expression in broiler chicken, Tropical Animal Health and Production, 51, 2279-2286

    Article  PubMed  Google Scholar 

  • Samanta, S., Haldar, S. and Ghosh, T., 2010. Comparative efficacy of an organic acid blend and bacitracin methylene disalicylate as growth promoters in broiler chickens: Effects on performance, gut histology, and small intestinal milieu, Veterinary medicine international, 2010, 645150

    Article  PubMed  Google Scholar 

  • Samli, H.E., Senkoylu, N., Koc, F., Kanter, M. and Agma, A., 2007. Effects of Enterococcus faecium and dried whey on broiler performance, gut histomorphology and intestinal microbiota, Archives of animal nutrition, 61, 42-49

    Article  PubMed  Google Scholar 

  • Sangilimadan, K., Richard Churchil, R., Premavalli, K. and Omprakash, A., 2019. Effect of Garlic (Allium sativum) on Production Performances and Carcass Traits of Nandanam Broiler-2, International Journal of Current Microbiology and Applied Sciences, 8, 2531-2538

    Article  CAS  Google Scholar 

  • Shang, A., Cao, S.-Y., Xu, X.-Y., Gan, R.-Y., Tang, G.-Y., Corke, H., Mavumengwana, V. and Li, H.-B., 2019. Bioactive compounds and biological functions of garlic (Allium sativum L.), Foods, 8, 246

    Article  CAS  PubMed Central  Google Scholar 

  • Siddiqui, S., Rahman, M., Islam, S., Islam, S., Hasan, M.M.I. and Rahman, M.M., 2017. Biological effects of commercial enzymes, probiotics and liver tonic on live weight and hematobiochemical parameters in broiler, International Journal of Research in Agricultural Sciences, 4, 56-59

    Google Scholar 

  • Sohail, M.U., Ijaz, A., Yousaf, M., Ashraf, K., Zaneb, H., Aleem, M. and Rehman, H., 2010. Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: Dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity, Poultry science, 89, 1934-1938

    Article  CAS  PubMed  Google Scholar 

  • Sohail, M., Hume, M., Byrd, J., Nisbet, D., Ijaz, A., Sohail, A., Shabbir, M. and Rehman, H., 2012. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress, Poultry science, 91, 2235-2240

    Article  CAS  PubMed  Google Scholar 

  • Song, J., Xiao, K., Ke, Y., Jiao, L., Hu, C., Diao, Q., Shi, B. and Zou, X., 2014. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress, Poultry science, 93, 581-588

    Article  CAS  PubMed  Google Scholar 

  • St-Pierre, N., Cobanov, B. and Schnitkey, G., 2003. Economic losses from heat stress by US livestock industries, Journal of dairy science, 86, E52-E77

    Article  Google Scholar 

  • Sugiharto, S., 2016. Role of nutraceuticals in gut health and growth performance of poultry, Journal of the Saudi Society of Agricultural Sciences, 15, 99-111

    Article  Google Scholar 

  • Varasteh, S., Braber, S., Akbari, P., Garssen, J. and Fink-Gremmels, J., 2015. Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides, PloS one, 10, e0138975

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, Y. and Gu, Q., 2010. Effect of probiotic on growth performance and digestive enzyme activity of Arbor Acres broilers, Research in Veterinary Science, 89, 163-167

    Article  CAS  PubMed  Google Scholar 

  • Xiao, Y., Xiang, Y., Zhou, W., Chen, J., Li, K. and Yang, H., 2017. Microbial community mapping in intestinal tract of broiler chicken, Poultry science, 96, 1387-1393

    Article  CAS  PubMed  Google Scholar 

  • Yazhini, P., Visha, P., Selvaraj, P., Vasanthakumar, P. and Chandran, V., 2018. Dietary encapsulated probiotic effect on broiler serum biochemical parameters, Veterinary world, 11, 1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yegani, M. and Korver, D., 2008. Factors affecting intestinal health in poultry, Poultry science, 87, 2052-2063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young, V.B., 2012. The intestinal microbiota in health and disease, Current opinion in gastroenterology, 28, 63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zubillaga, M., Weill, R., Postaire, E., Goldman, C., Caro, R. and Boccio, J., 2001. Effect of probiotics and functional foods and their use in different diseases, Nutrition Research, 21, 569-579

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge their respective universities and institutes for their cooperation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Abdel-Moneim Eid Abdel-Moneim.

Ethics declarations

Ethical approval

All the procedures used in this trial were approved by the Local Experimental Animals Care and Welfare Committee and approved by the Institutional Ethics Committee.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Elbaz, A.M., Ibrahim, N.S., Shehata, A.M. et al. Impact of multi-strain probiotic, citric acid, garlic powder or their combinations on performance, ileal histomorphometry, microbial enumeration and humoral immunity of broiler chickens. Trop Anim Health Prod 53, 115 (2021). https://doi.org/10.1007/s11250-021-02554-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11250-021-02554-0

Keywords

Navigation