بررسی اثرات پروبیوتیک بومی بر عملکرد، پاسخ ایمنی، ریخت‌شناسی و جمعیت لاکتوباسیلوسی روده جوجه‌های گوشتی

نوع مقاله : مقاله پژوهشی

نویسندگان

1 پژوهشکده بیوتکنولوژی جانوری، پژوهشگاه بیوتکنولوژی کشاورزی ایران (ABRII)، سازمان تحقیقات، آموزش و ترویج کشاورزی (AREEO)

2 پژوهشکده بیو تکنو لوژی جانوری کشور، پژوهشکده بیوتکنولوژی کشاورزی ایران (ABRII)، سازمان تحقیقات، آموزش و ترویج کشاورزی

3 گروه علوم دامی، دانشکده کشاورزی، دانشگاه گیلان، رشت، ایران

چکیده

هدف از انجام پژوهش حاضر، بررسی تأثیر پروبیوتیک‌های بومی شامل لاکتوباسیلوس روترئی و لاکتوباسیلوس سالیواریوس جدا‌شده از مرغ‌ها و اردک بومی به‌صورت سویه‌های تکی (Plr2) و ترکیبی (Plr9, Plr10, Plr11, Plr12) بر ویژگی‌های عملکردی، پاسخ ایمنی و جمعیت لاکتوباسیلوسی روده در 512 جوجه گوشتی نر نژاد راس 308 بود. نتایج نشان داد که از نظر میزان خوراک مصرفی، افزایش وزن روزانه و ضریب تبدیل تفاوت معنی‌داری بین تیمارهای پروبیوتیکی مورد استفاده مشاهده نشد. بررسی آنتی‌بادی تولیدی علیه SRBC تزریق‌شده در 30 روز اول پرورش نشان داد که ترکیب پروبیوتیکی Plr12 منجر به افزایش معنی‌داری IgG در مقایسه با شاهد گردید (01/0>P). پاسخ ثانویه در افزایش میزان این آنتی‌بادی در 42 روز پس از تزریق SRBC با قدرت بیشتری همراه بود و در تمام ترکیبات پروبیوتیکی مورد استفاده به‌طور معنی‌داری نسبت به شاهد مشاهده گردید (01/0>P). بررسی جمعیت لاکتوباسیلوسی سکوم جوجه‌های گوشتی مورد مطالعه نیز حاکی از آن بود که سویه‌های ترکیبی Plr9، Plr11 و Plr12 سبب افزایش معنی‌دار جمعیت این باکتری‌های مفید در مقایسه با شاهد و بیوپول (پروبیوتیک تجاری) گردید (01/0>P). مطالعه حاضر مشخص کرد که باکتری‌های با قابلیت پروبیوتیکی جدا‌شده از جمعیت میکروبی موجود در دستگاه گوارش طیور بومی، چه به‌صورت تکی و چه در ترکیب با هم این پتانسیل را دارند که به‌عنوان یک مکمل غذایی باارزش، جایگزین آنتی‌بیوتیک‌ها و پروبیوتیک‌های تجاری در تغذیه طیور شوند.

کلیدواژه‌ها

موضوعات

عنوان مقاله [English]

Investigation of the Effects of Native Probiotics on the Performance, Immune Response, Morphology, and Intestinal Lactobacillus Population in Broiler Chicks

نویسندگان [English]

  • Ramin Seighalani 1
  • Maryam Royan 2
  • Majid Mottaghitalab 3
  • fatemeh zare 1
1 Agricultural Biotechnology Research Institute of Iran (ABRII), North Region Branch, Agricultural Research, Education and Extension Organization (AREEO)
2 Assistant Professor , Institute of Animal Biotechnology, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO), Rasht, Iran
3 Dept. of Animal Science, Faculty of agri., Uni, of Guilan, Rasht, Iran
چکیده [English]

Introduction: Various factors have been reported to influence broiler chicken performance, including environmental conditions, nutrition, management practices, and genetics. One of the priorities in poultry production is the availability of effective alternatives to antibiotics, and the native strains of this type of alternative have various advantages. Probiotics as live microbial supplements in feed improve the microbial balance of the gastrointestinal tract and then improve animal health. Probiotics can enhance growth performance, support the immune system, aid nutrient digestion, and positively influence the microbial population of the gastrointestinal tract. Commercial probiotics are the most commonly used; however, screening the natural flora of the gastrointestinal tract has become a valuable approach in identifying effective probiotic strains. Selecting the optimal species for use in probiotic supplements is largely experimental and depends on their proven impact on the performance of living organisms. This project aimed to investigate the effects of indigenous probiotics on broiler chickens.
Materials and Methods: The probiotics included strains of Lactobacillus reuteri isolated from native chickens in Oshnavieh, Shush, Shaft, and Masal, as well as Lactobacillus salivarius isolated from native ducks in Mazandaran. The study aimed to assess the impact of these probiotics on the performance, immune response, morphology, and gut lactobacillus population in broiler chickens. The single strain (Plr2) and combination strains (Plr9, Plr10, Plr11, and Plr12) were evaluated in a completely randomized design. There were seven treatments, each with four replicates, and 16 one-day-old Ross 308 broiler chickens per replicate. Treatments include 1) control: basic diet without any additive, 2) Positive control 2: basic diet + commercial probiotic, 3) Basic ration + 1.36×109 CFU/g L. Reuteri isolated from Oshnavieh native hen (Plr2), 4) Basic ration + 1.36×109 CFU/g L. Reuteri isolated from Oshnavieh native hen and L. salivarius isolated from Mazandaran native duck (Plr9), 5) Basic ration + 1.36×109 CFU/g L. Reuteri isolated from Oshnavieh native hen and L. salivarius isolated from Mazandaran native duck and L. Reuteri isolated from Shush native hen (Plr10), 6) Basic ration + 1.36×109 CFU/g L. Reuteri isolated from Oshnavieh native hen and L. salivarius isolated from Mazandaran native duck and L. Reuteri isolated from Shush native hen and L. Reuteri isolated from Shaft native hen (Plr11) and 7) Basic ration + 1.36×109 CFU/g L. Reuteri isolated from Oshnavieh native hen and L. salivarius isolated from Mazandaran native duck and L. Reuteri isolated from Shush native hen and L. Reuteri isolated from Shaft native hen and L. Reuteri isolated from Masal native hen (Plr12).
Results and Discussion: There were no significant differences in feed intake, daily weight gain, or feed conversion ratio among the probiotic treatment groups. However, evaluation of antibody production against sheep red blood cells (SRBC) injected during the first 30 days of rearing showed that the Plr12 probiotic combination significantly increased IgG levels compared to the control group (without additives). The secondary immune response, measured 42 days after SRBC injection, showed an even greater increase in antibody levels. Additionally, all probiotic combinations significantly enhanced antibody levels compared to the control. It appears that as the chicks mature, their immune system continues to develop, and the memory cells generated during the initial immune response led to an increased production of antibodies during the subsequent response. Results derived from the broilers jejunum morphology study in the first experiment showed that the addition of the native probiotic combination Plr9, Plr11, and Plr12 to the diet resulted in a significant increase in the length of the intestinal villi of jejunum in chickens from the experimental groups when compared to chickens from the control group. Also, investigation of villus length/crypt depth and surface villus area indicated a significant increase in these traits in all probiotic treatments used compared to control treatments and commercial probiotic. The examination of the lactobacillus population in the cecal contents of broiler chickens showed that the combination of strains Plr9, Plr11, and Plr12 significantly increased the population of these beneficial bacteria compared to the control and commercial probiotic treatments. Each strain had specific probiotic properties. When these strains were combined and administered to broiler chickens, there was a significant increase in beneficial bacteria and a reduction in harmful bacteria.
Conclusions: This study demonstrates that probiotic bacteria, isolated from the microbial population of the digestive system of native birds, have the potential to serve as valuable dietary supplements in poultry nutrition. Each probiotic strain confers varying levels of optimal efficacy; as a result, these probiotics can be used individually or in combination, and they can replace antibiotics and commercial probiotics.

کلیدواژه‌ها [English]

  • Broiler chicken
  • Immnune response
  • Intestinal morphology
  • Microbial population
  • Probiotic

©2023 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source.

 

 https://doi.org/10.22067/ijasr.2024.88990.1209

مراجع

  1. Ahmed, S. , Hoon, J., Mun, H. S., & Yang, C. J. (2014). Evaluation of Lactobacillus and Bacillus-based probiotics as alternatives to antibiotics in enteric microbial challenged weaned piglets. African Journal of Microbiology Research, 8(1), 96-104. https://doi.org/10.5897/AJMR2013.6355
  2. Alagawany, M., Abd El-Hack, M. E., Farag, M. R., Sachan, S., Karthik, K., & Dhama, K. (2018). The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environmental Science Pollution Reserch, 25, 10611-10618. https://doi.org/1007/s11356-018-1687-x
  3. Amir Ebrahimi, N., Salehi Jouzani, G., & Ebrahimi, M. A. (2022). Native chicken-derived Lactobacillus strains with high probiotic, cholesterol-assimilation and aflatoxin-degradation capabilities. Iranian Journal of Microbiology, 14(2), 227–237. https://doi.org/10.18502/ijm.v14i2.9192
  4. Apata, D. F. (2008). Growth performance, nutrient digestibility and immune response of broiler chicks fed diets supplemented with a culture of Lactobacillus bulgaricus. Journal of the Science of Food and Agriculture, 88(7), 1253-1258. https://doi.org/1002/jsfa.3214
  5. Asadi, A., Faeleh, H., & Razzaghzadeh, S. (2019). Effect of given probiotic type on broiler chicken performance and carcass properties. Applied Research in Animal Science, 31, 51-58. https://doi.org/22092/aasrj.2019.123658.1164
  6. Awad, W. A., Böhm , J., Razzazi-Fazeli, E., Ghareeb, K., & Zentek, J. (2006). Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poultry Science, 85(6), 974-979. https://doi.org/10.1093/ps/85.6.974
  7. Awad, W., Ghareeb, K., & Böhm, J. (2008). Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides. Italian Journal of Molecular Science, 9, 2205-2216. https://doi.org/3390/ijms9112205
  8. Awais, M. M., Jamal, M. A., Akhtar, M., Hameed, M. R., Anwar, M. I., & Ullah, M. I. (2019). Immunomodulatory and ameliorative effects of Lactobacillus and Saccharomyces based probiotics on pathological effects of eimeriasis in broilers. Microbiology Pathogen, 126, 101-108. https://doi.org/1016/j.micpath.2018.10.038
  9. Bai, S. P., Wu, A. M., Ding, X. M., Lei, Y., Bai, J., Zhang, K. Y., & Chio, J. S. (2013). Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poultry Science, 92(3), 663-670. https://doi.org/3382/ps.2012-02813
  10. Bilal, M., Si, W., Barbe, F., Chevaux, E., Sienkiewicz, O., & Zhao, X. (2021). Effects of novel probiotic strains of Bacillus pumilus and Bacillus subtilis on production, gut health, and immunity of broiler chickens raised under suboptimal conditions. Poultry Science, 100(3), 100871. https://doi.org/1016/j.psj.2020.11.048
  11. Broom, L. J., & Kogut, M. H. (2018). The role of the gut microbiome in shaping the immune system of chickens. Veterinary Immunology and Immunopathology, 204, 44-51. https://doi.org/1016/j.vetimm.2018.10.002
  12. Chen, F., Zhu, L., & Qiu, H. (2017). Isolation and probiotic potential of Lactobacillus salivarius and Pediococcus pentosaceus in specific pathogen free chickens. Brazilian Journal of Poultry Science, 19, 325-332. https://doi.org/1590/1806-9061-2016-0413
  13. Cisek, A. A., & Binek, M. (2014). Chicken intestinal microbiota function with a special emphasis on the role of probiotic bacteria. Polish Journal of Veterinary Sciences, 17(2), 385-394. https://doi.org/2478/pjvs-2014-0057
  14. Chamani, M. (2016). Efficacy of Bactocell® and Toyocerin® as probiotics on growth performance, blood parameters and intestinal morphometry of turkey poults. Iranian Journal of Applied Animal Science, 6, 211-218. (In Persion).
  15. Clavijo, V., & Flórez, M. J. V. (2018). The gastrointestinal microbiome and its association with the control of pathogens in broiler chicken production: A review. Poultry Science, 97(3), 1006-1021. https://doi.org/10.3382/ps/pex359
  16. Dibner, J. J., & Richards, J. D. (2005). Antibiotic growth promoters in agriculture: History and mode of action. Poultry Science, 84(4), 634-643. https://doi.org/10.1093/ps/84.4.634
  17. Ebrahimi, E., Sobhani, R. S., & Zarghi, H. (2017). Effect of triticale level and exogenous enzyme in the grower diet on performance, gastrointestinal tract relative weight, jejunal morphology and blood lipids of Japanese quality. Journal of Agricultural Science Technology, 19, 569-580. http://dorl.net/dor/20.1001.1.16807073.2017.19.3.3.2
  18. Ehsani Tabatabaeii, F., & Pourrahimi, F. (2015). Cell Biology Laboratory. Payame Noor University Press, Iran. pp. 121-134. (In Persion).
  19. Elbaz, A. M., Ibrahim, N. S., Shehata, A. M., Mohamed, N. G., & Abdel-Moneim, A. E. (2021). Impact of multi-strain probiotic, citric acid, garlic powder or their combinations on performance, ileal histomorphometry, microbial enumeration and humoral immunity of broiler chickens. Tropical Animal Health and Production, 53(1), 115. https://doi.org/10.1007/s11250-021-02554-0
  20. Fazelnia, K., Fakhraei, J., Yarahmadi, H. M., & Amini, K. (2021). Dietary supplementation of potential probiotics Bacillus subtilis, Bacillus licheniformis, and Saccharomyces cerevisiae and synbiotic improves growth performance and immune responses by modulation in intestinal system in broiler chicks challenged with Salmonella typhimurium. Probiotics Antimicrobial Proteins, 13(4), 1081-1092. https://doi.org/1007/s12602-020-09737-5
  21. Fuentes, C., Orozco, L., Vicente, J., Velasco, X., & Menconi, A. (2013). Effect of a lactic acid bacteria based probiotic, Floramax-B11®, on performance, bone qualities, and morphometric analysis of broiler chickens: an economic analysis. Biological Systems, 2(113), 2.
  22. Gadde, U., Kim, W. H., Oh, S. T., & Lillehoj, H. S. (2017). Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: A review. Animal Health Research Review, 18, 26-45. https://doi.org/1017/S1466252316000207
  23. Gangali, H., Raji, A. R., & Zarghi, H. (2015). Effect of post hatch delayed access to feed on performance, GIT physical and histological development and yolk absorption in young broiler chicks. Biomedical Pharmacology Journal, 8, 945-955. https://doi.org/1016/j.psj.2020.06.023
  24. Grasman, K. A. (2010). In vivo functional test for assessing immunotoxicity in birds. Methods in Molecular Biology, 598, 387-398. https://doi.org/10.1007/978-1-60761-401-2_25.
  25. Hack, M. E. A., Saadony, M. T., Shafi, M. E., Qattan, S. Y. A., Batiha, G. E., Khafaga, A. F., Moneim, A. M. E., & Alagawany, M. (2020). Probiotics in poultry feed: a comprehensive review. Journal of Animal Physiology and Animal Nutrition, 104(6), 1835-1850. https://doi.org/1111/jpn.13454
  26. Haghighi, H. R., Gong, J., Gyles, C. L., Hayes, M. A., Sanei, B., Parvizi, P., Gisavi, H., Chambers, J. R., & Sharif, S. (2005). Modulation of antibody-mediated immune response by probiotics in chickens. Clinical and Diagnostic Laboratory Immunology, 12(12), 1387-1392. https://doi.org/10.1128/CDLI.12.12.1387-1392.2005
  27. He, T., Long, S., Mahfuz, S., Wu, D., Wang, X., Wei, X., & Piao, X. (2019). Effects of probiotics as antibiotics substitutes on growth performance, serum biochemical parameters, intestinal morphology, and barrier function of broilers. Animals, 9, 985-995. https://doi.org/3390/ani9110985
  28. Huang, T., Peng, X. Y., Gao, B., Wei, Q. L., Xiang, R., Yuan, M. G., & Xu, Z. H. (2019). The effect of Clostridium butyricum on the gut microbiota, immune response and intestinal barrier function during the development of necrotic enteritis in chickens. Frontiers Microbiology, 10, 2309. https://doi.org/3389/fmicb.2019.02309
  29. Jacquier, V., Nelson, A., Jlali, M., Rhayat, L., Brinch, K. S., & Devillard, E. (2019). Bacillus subtilis 29784 induces a shift in broiler gut microbiome toward butyrate producing bacteria and improves intestinal histomorphology and animal performance. Poultry Science, 98, 2548-2554. https://doi.org/3382/ps/pey602
  30. Jadhav, K., Katoch, S., Sharma, K., & Mane, B. G. (2015). Probiotics in broiler poultry feeds: A review. Journal of Animalal Nutrition Physiology, 1, 4-16.
  31. Jing, G. C., Jing, G., Sun, Z., Wang, H., Gong, Y., Huang, S., Ning, K., XU, J., & SU, X. (2017). Parallel META 3: Comprehensive taxonomical and functional analysis platform for efficient comparison of microbial communities. Scientific Reports, 7, 40371. https://doi.org/10.1038/srep40371
  32. Khalid, A. H., Ullah, K. S., Naveed, S., Latif, F., Pasha, T. N., Hussain, I., & Qaisrani, S. N. (2021). Effects of spray dried yeast (Saccharomyces cerevisiae) on growth performance and carcass characteristics, gut health, cecal microbiota profile and apparent ileal digestibility of protein, amino acids and energy in broilers. Tropical Animal Health and Production, 8(53), 252-263. https://doi.org/10.1007/s11250-021-02684-5
  33. Kulkarni, R. R., Gaghan, C., Gorrell, K., Sharif, S., & Taha-Abdelaziz, K. (2022). Probiotics as alternatives to antibiotics for the prevention and control of Necrotic Enteritis in chickens. Pathogens, 11(6), 692. https://doi.org/10.3390/pathogens11060692
  34. Lajis, A. F. B. (2020). Biomanufacturing process for the production of bacteriocins from Bacillaceae family. Bioresource Bioprocess, 7(8). https://doi.org/1186/s40643-020-0295-z
  35. Lei, X., Piao, X., Ru, Y., Zhang, H., Péron, A., & Zhang, H. (2015). Effect of Bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian-Australasian Journal of Animal Science, 28(2), 239-246. https://doi.org/5713/ajas.14.0330
  36. Li, Y. B., Xu, Q. Q., Yang, C. J., Yang, X., Lv, L., Yin, C. H., & Yan, H. (2014). Effects of probiotics on the growth performance and intestinal micro flora of broiler chickens. Pakistan Journal of Pharmaceutical Sciences, 27, 713-717.
  37. Ma, K., Chen, W., Yan, S. Q., Liu, Z. Z., Lin, X. Q., Zhang, J. B., Gao, Y., Wang, T., Zhang, J. G., & Yang, Y. J. (2022). Purification, characterization, mode of action, and application of Jileicin, a novel antimicrobial from Paenibacillus jilinensis Journal of Agriculture and Food Chemistry, 70(18), 5570-5578. https://doi.org/10.1021/acs.jafc.2c01458
  38. Ma, Y., Wang, W., Zhang, H., Wang, J., Zhang, W., Gao, J., Wu, S., & Qi, G. (2018). Supplemental Bacillus subtilis DSM 32315 manipulates intestinal structure and microbial composition in broiler chickens. Science Reports, 8, 15358. https://doi.org/1038/s41598-018-33762-8
  39. Mahmood Tabar, A., Amir Karimi Torshizi, M., Sharafi, M., & Mozhgani, N. (2018). The effect of some poultry probiotics produced in Iran on performance parameters, economic indices and small intestinal morphology of broilers. Iranian Journal of Animal Science, 49(3), 415-425. (In Persion).
  40. Mikulski, D. 1., Jankowski, J., Naczmanski, J., Mikulska, M., & Demey, V. (2012). Effects of dietary probiotic (Pediococcus acidilactici) supplementation on performance, nutrient digestibility, egg traits, egg yolk cholesterol, and fatty acid profile in laying hens. Poultry science, 91(10), 2691-2700. https://doi.org/10.3382/ps.2012-02370
  41. Montagne, L., Pluske, J. R., & Hampson, D. H. (2003). A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Animal Feed Science Technology, 108, 95-117. https://doi.org/1016/S0377-8401(03)00163-9
  42. Mookiah, S., Sieo, C. C., Ramasamy, K., Abdullah, N., & Ho, Y. W. (2014). Effects of dietary prebiotics, probiotic and synbiotics on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens. Journal of the Science of Food and Agriculture, 94(2), 341-348. https://doi.org/1002/jsfa.6365
  43. Nain, S. Renema, R. A., Zuidhof, M. J., & Korver, D. R. (2012). Effect of metabolic efficiency and intestinal morphology on variability in n-3 polyunsaturated fatty acid enrichment of eggs. Poultry Science, 91, 888-898. https://doi.org/3382/ps.2011-01661
  44. Nakphaichit, M., Thanomwongwattana, S., Phraephaisarn, C., Sakamoto, N., Keawsompong, S., Nakayama, J., & Nitisinprasert, S. (2011). The effect of including Lactobacillus reuteri KUB-AC5 during post-hatch feeding on the growth and ileum microbiota of broiler chickens. Poultry Science, 90(12), 2753-2765. https://doi.org/3382/ps.2011-01637
  45. Ohimain, E. I., & Ofongo, R. T. (2012). The effect of probiotic and prebiotic feed supplementation on chicken health and gut microflora: a review. International Journal of Animal and Veterinary Advances, 4(2), 135-143.
  46. Rastad, A. H., Samie, A., & Daneshvar, F. (2008). Effect of Bactocell and dry whey on performance and carcass characteristics of broiler chickens. Journal of Crop Production and Processing, 12(43), 473-480. (In Persion)
  47. Rehman, A., Arif, M., Sajjad, N., Al-Ghadi, M. Q., Alagawany, M., Abd El-Hack, M. E., Alhimaidi, A. R., Elnesr, S. S., Almutairi, B. O., Amran, R. A.; Hussein, E. O. S., & Swelum, A. A. (2020). Dietary effect of probiotics and prebiotics on broiler performance, carcass, and immunity. Poultry Science, 99(12), 6946-6953. https://doi.org/10.1016/j.psj.2020.09.043
  48. Royan, M., Alaie Kordghashlaghi, H., Afraz, F., Hashemi, M., Vahidi, S. M. F., & Seighalani, R. (2017). Screening Lactobacilli isolates from Northern Iran Backyard chickens as bio-control strategy against Salmonella enteritidis and Salmonella typhimurium. Kafkas Universitesi Veteriner Fakultesi Dergisi, 24(3), 423-430. https://doi.org/10.9775/kvfd.2017.19109
  49. Samanya, M., & Yamauchi, K. (2002). Histological alterations of intestinal villi in chickens fed dried Bacillus subtilis. var. natto. Comparative Biochemistry and Physiology, 133, 95-104. https://doi.org/1016/s1095-6433(02)00121-6
  50. Sarangi, N. R., Babu, L. K., Kumar, A., Pradhan, C. R., Pati, P. K., & Mishra, J. P. (2016). Effect of dietary supplementation of prebiotic, probiotic, and synbiotic on growth performance and carcass characteristics of broiler chickens. Veterinary World, 9, 313-319. https://doi.org/14202/vetworld.2016.313-319
  51. Shokryazdan, P., Faseleh, M., Jahromi, J. B., Liang, K., Ramasamy, C. C., & Ho, Y. W. (2017). Effects of Lactobacillus salivarius mixture on performance, intestinal health and serum lipids of broiler chickens. PLoS ONE, 12(5), e0175959. https://doi.org/1371/journal.pone.0175959
  52. Soomro, R. N., Abd El-Hack, M. E., Shah, S. S., Taha, A. E., Alagawany, M., Swelum, A. A., Hussein, E. O. S., Ba-Aawdh, H. A., Saadeldin, I., El-Edel M. A., & Tufarelli, V. (2019). Impact of restricting feed and probiotic supplementation on growth performance, mortality and carcass traits of meat-type quails. Animal Science Journal, 90, 1388-1395. https://doi.org/1111/asj.13290
  53. Terada, T., Nii, T., Isobe, N., & Yoshimura, Y. (2020). Effects of probiotics Lactobacillus reuteri and Clostridium butyricum on the expression of toll-like receptors, pro- and anti-inflammatory cytokines, and antimicrobial peptides in broiler chick intestine. The Journal of Poultry Science, 57(4), 310-318. https://doi.org/2141/jpsa.0190098
  54. Timmerman, H. M., Veldman, A., Van den Elsen, E., Rombouts, F. M., & Beynen, A. C. (2006). Mortality and growth performance of broilers given drinking water supplemented with chicken-specific probiotics. Poultry Science, 85(8), 1383-1388. https://doi.org/10.1093/ps/85.8.1383
  55. Van Immerseel, F., Russell, J. B., Flythe, M. D., Gantois, I., Timbermont, L., Pasmans, F., Haesebrouck, F., & Ducatelle, R. (2006). The use of organic acids to combat Salmonella in poultry: A mechanistic explanation of the efficacy. Avian Pathology, 35(3), 182-188. https://doi.org/10.1080/03079450600711045
  56. Van Zyl, W. F., Deane, S. M., & Dicks, L. M. T. (2020). Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria. Gut Microbes, 12(1), 1831339. https://doi.org/1080/19490976.2020.1831339
  57. Villena, J., Medina, M., Vinti˜ni, E., & Alvarez, S. (2008). Stimulation of respiratory immunity by oral administration of Lactococcus lactis. Canadian Journal of Microbiology, 54(8), 630-638. https://doi.org/1139/W08-052
  58. Zhang, Z. F., & Kim, I. H. (2014). Effects of multistrain probiotics on growth performance, apparent ileal nutrient digestibility, blood characteristics, cecal microbial shedding, and excreta odor contents in broilers. Poultry Science, 93(2), 364-370. https://doi.org/10.3382/ps.2013-03314
  59. Zhang, L., Zhang, R., Jia, H., Zhu, Z., Li, H., & Ma, Y. (2021). Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens. Open Life Science, 16, 311-322. https://doi.org/1515/biol-2021-0031
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  • تاریخ دریافت: 31 تیر 1403
  • تاریخ بازنگری: 04 دی 1403
  • تاریخ پذیرش: 08 دی 1403
  • تاریخ اولین انتشار: 08 دی 1403

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