Blood and Intestine Profile of Broilers Fed Averrhoa bilimbi Fruit, Wheat Bran, and Yeast Blends
Abstract
A. bilimbi fruit filtrate, wheat bran, and S. cerevisiae contain bioactive components favorable to broiler health. The use of these compounds in combination was expected to exert synergistic effects on broilers. The study investigated the effect of a combination of A. bilimbi fruit filtrate, wheat bran, and S. cerevisiae on haematological indices and intestinal selected bacteria and morphology of broilers. A total of 280 broiler chicks were randomly divided into 4 groups with 7 replications, including CONT (chicks offered diet without additive), TBLEND1, BLEND2, and BLEND3 (chicks offered diet with 0.25%, 0.5%, and 1% of the additive combination of A. bilimbi fruit filtrate, wheat bran, and S. cerevisiae), respectively. For data collection, the chicks were blood sampled at day 21 and 35, and slaughtered at day 35. The data were statistically treated with analysis of variance according to a completely randomized design. On day 21, the erythrocytes and haemoglobin levels were lower in BLEND2 and BLEND3 than those in CONT and BLEND1 (p<0.05). The leukocytes and lymphocytes values were lower in BLEND2 and BLEND3 than those in CONT (p<0.05). On day 35, erythrocytes were lower (p<0.05) in BLEND3 than that in CONT and BLEND1. The increased additive levels linearly decreased (p<0.05) erythrocytes, haemoglobin, and haematocrits values. At day 21, total triglyceride was lower (p<0.05) in BLEND3 than that in BLEND1 and BLEND2. The LDL level was lower (p<0.05) in BLEND3, whereas the HDL level was higher (p<0.05) in CONT than that in other groups. Creatinine was higher (p<0.05) in BLEND3 than in other groups. The ileal lactose negative Enterobacteriaceae counts were lower in BLEND1, BLEND2, and BLEND3 than in CONT (p<0.05). The duodenal villi height to crypt depth ratio (VH/CD ratio) was higher (p<0.05) in BLEND1 than that in CONT and BLEND2. In the ileum, the VH/CD ratio linearly increased (p<0.05) with the elevated additive levels. In conclusion, the combination of A. bilimbi fruit filtrate, wheat bran, and S. cerevisiae was beneficial in reducing intestinal pathogen load and improving intestinal morphology of broilers.
References
Abdel-Sattar, W. M., K. M. Sadek, A. R. Elbestawy, & D. M. Mourad. 2019. The protective role of date palm (Phoenix dactylifera seeds) against aflatoxicosis in broiler chickens regarding carcass characteristics, hepatic and renal biochemical function tests and histopathology. World Vet. J. 9:59-69. https://doi.org/10.36380/scil.2019.wvj9
Abudabos, A. M., A. H. Alyemni, Y. M. Dafalla, & R. U. Khan. 2017. The effect of phytogenics on growth traits, blood biochemical and intestinal histology in broiler chickens exposed to Clostridium perfringens challenge. J. Appl. Anim. Res. 46:691-695. https://doi.org/10.1080/09712119.2017.1383258
Aka-Tanimo, H. A., D. O. Oshibanjo, V. O. Adelowo, M. A. Akwashiki, I. W. Azi, O. C. James, S. Haruna, & A. Y. Sunday. 2020. Growth performance, carcass characteristics and hematology indices of broiler chicken fed graded levels of (Mangifera indica) mango leaf meal. Asian J. Res. Anim. Vet. Sci. 6:20-27.
Akhtar, M., M. M. Awais, M. I. Anwar, S. Ehtisham-ulHaque, A. Nasir, M. K. Saleemi, & K. Ashraf. 2015. The effect of infection with mixed Eimeria species on hematology and immune responses following Newcastle disease and infectious bursal disease booster vaccination in broilers. Vet. Q. 35:21-26. https://doi.org/10.1080/01652176.2014.991048
Alaqil, A. A., A. O. Abbas, H. S. El-Beltagi, H. El-Atty, K. Abd, G. M. Mehaisen, & E. S. Moustafa. 2020. Dietary supplementation of probiotic Lactobacillus acidophilus modulates cholesterol levels, immune response, and productive performance of laying hens. Animals 10:1588. https://doi.org/10.3390/ani10091588
Asheg, A., M. Levkut, V. Revajova, Z. Sevcikova, L. Kolodzieyski, & J. Pistl. 2002. T lymphocyte subpopulations and B lymphocyte cells in caecum and spleen of chicks infected with Salmonella enteritidis. Acta Histochem. 104:435-439. https://doi.org/10.1078/0065-1281-00666
Awad, W. A., K. Ghareeb, S. Abdel-Raheem, & J. Böhm, J. 2009. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult. Sci. 88:49-56. https://doi.org/10.3382/ps.2008-00244
Bolton, W. 1967. Poultry Nutrition. MAFF Bulletin No.174. HMSO, London.
Cimrin, T., R. I. Tunca, M. D. Avsaroglu, T. Ayasan, & S. Kücükersan. 2020. Effects of an antibiotic and two phytogenic substances (cinnamaldehyde and 1,8-cineole) on yolk fatty acid profile and storage period-associated egg lipid peroxidation level. R. Bras. Zootec. 49:e20190270. https://doi.org/10.37496/rbz4920190270
Del Vesco, A. P., E. Gasparino, D. O. Grieser, V. Zancanela, D. M. Voltolini, A. S. Khatlab, S. E. F. Guimarães, M. A. M. Soares, & A. R. O. Neto. 2015. Effects of methionine supplementation on the expression of protein deposition-related genes in acute heat stress-exposed broilers. PLoS ONE 10:e0115821. https://doi.org/10.1371/journal.pone.0115821.t002
Elghandour, M. M. Y., Z. L. Tan, S. H. Abu Hafsa, M. J. Adegbeye, R. Greiner, E. A. Ugbogu, J. C. Monroy, & A. Z. M. Salem. 2019. Saccharomyces cerevisiae as a probiotic feed additive to non and pseudo‐ruminant feeding: A review. J Appl. Microbiol. 128:658-674. https://doi.org/10.1111/jam.14416
Feng, Y., L. Wang, A. Khan, R. Zhao, S. Wei, & X. Jing. 2020. Fermented wheat bran by xylanase-producing Bacillus cereus boosts the intestinal microflora of broiler chickens. Poult. Sci. 99:263-271. https://doi.org/10.3382/ps/pez482
Fumagalli, S., F. Fattirolli, L. Guarducci, T. Cellai, S. Baldasseroni, F. Tarantini, D. Di Bari, G. Masotti, & N. Marchionni. 2011. Coenzyme Q10 terclatrate and creatine in chronic heart failure: a randomized, placebo-controlled, double-blind study. Clin. Cardiol. 34:211-7. https://doi.org/10.1002/clc.20846
Gunenc, A., C. Alswiti, & F. Hosseinian. 2017. Wheat bran as a prebiotic source and antioxidant activities of fiber fractions. J. Food Res. 6:1-10. https://doi.org/10.5539/jfr.v6n2p1
He, T., S. Mahfuz, X. Piao, D. Wu, W. Wang, H. Yan, T. Ouyang, & Y. Liu. 2021. Effects of live yeast (Saccharomyces cerevisiae) as a substitute to antibiotic on growth performance, immune function, serum biochemical parameters and intestinal morphology of broilers. J. Appl. Anim. Res. 49:15-22. https://doi.org/10.1080/09712119.2021.1876705
Helal, F., A. El-Badawi, S. El-Naggar, M. Shourrap, O. Aboelazab, & S. A. Hafsa. 2021. Probiotics role of Saccharomyces cerevisiae and Bacillus subtilis in improving the health status of rabbits’ gastrointestinal tract. Bull. Natl. Res. Cent. 45:1-9. https://doi.org/10.1186/s42269-021-00522-0
Hidanah, S., E. K. Sabdoningrum, R. S. Wahjuni, & S. Chusniati. 2018. Effects of meniran (Phyllanthus niruri L.) administration on leukocyte profile of broiler chickens infected with Mycoplasma gallisepticum. Vet. World. 11:834-839. https://doi.org/10.14202/vetworld.2018.834-839
Józefiak, D., S. Kaczmarek, & A. Rutkowski. 2008. A note on the effects of selected prebiotics on the performance and ileal microbiota of broiler chickens. J. Anim. Feed Sci. 17:392-397. https://doi.org/10.22358/jafs/66633/2008
Kırkpınar, F., Z. Açıkgöz, S. Mert, & O. Işık. 2018. Effects of dietary probiotic, prebiotic and enzyme mixture supplementation on performance, carcass, organ, ileal pH and viscosity of broilers. J. Anim. Prod. 59:1-9. https://doi.org/10.29185/hayuretim.469862
Konjufca, V. H., G. M. Pesti, & R. B. Bakalli. 1997. Modulation of cholesterol levels in broiler meat by dietary garlic and copper. Poult. Sci. 76:1264-1271. https://doi.org/10.1093/ps/76.9.1264
Kostadinović, L. M., S. T. Pavkov, J. D. Lević, T. A. GalonjaCoghill, G. K. Dozet, & N. C. Bojat. 2011. Effect of sulphachloropyrazine on antioxidative systems in blood and liver of broilers. Acta Vet. Brno. 80:165-170. https://doi.org/10.2754/avb201180020165
Lan, R. X., S. Q. Li, Z. Zhao, & L. L. An. 2020. Sodium butyrate as an effective feed additive to improve growth performance and gastrointestinal development in broilers. Vet. Med. Sci. 6:491-499. https://doi.org/10.1002/vms3.250
Li, B., J. Leblois, B. Taminiau, M. Schroyen, Y. Beckers, J. Bindelle, & N. Everaert. 2018. The effect of inulin and wheat bran on intestinal health and microbiota in the early life of broiler chickens. Poult. Sci. 97:3156-3165. https://doi.org/10.3382/ps/pey195
Lin, W. C. & T. T. Lee. 2020. Laetiporus sulphureus-fermented wheat bran enhanced the broiler growth performance by improving the intestinal microflora and inflammation status. Poult. Sci. 99:3606-3616. https://doi.org/10.1016/j.psj.2020.04.011
Mareta, I., G. Nathaniel, T. Yudiarti, E. Widiastuti, H. I. Wahyuni, & S. Sugiharto. 2020. Effect of Averrhoa bilimbi fruit filtrate and shrimp paste mixture on performance, gut microbes and blood profile of broilers. Indonesian Journal of Animal and Veterinary Science 25:182-189. https://doi.org/10.14334/jitv.v25i4.2515
Morales-López, S., J. A. Yepes, J. C. Prada-Herrera, & A. Torres-Jiménez. 2019. Enterobacteria in the 21st century: a review focused on taxonomic changes. J. Infect. Dev. Ctries. 13:265-273. https://doi.org/10.3855/jidc.11216
Müller, M., G. D. A. Hermes, C. E. Emanuel, J. J. Holst, E. G. Zoetendal, H. Smidt, F. Troost, F. G. Schaap, S. O. Damink, J. W. E. Jocken, K. Lenaerts, A. A. M. Masclee, & E. E. Blaak. 2020. Effect of wheat bran derived prebiotic supplementation on gastrointestinal transit, gut microbiota, and metabolic health: a randomized controlled trial in healthy adults with a slow gut transit. Gut Microbes 12:1704141. https://doi.org/10.1080/19490976.2019.1704141
Nasr El-Deen, N. A. M., S. A. M. El-Mandrawy, & M. A. Mahmoud. 2018. Trial in using Clostridium butyricum as prophylactic for Salmonellosis in broiler chicken: Hemato-biochemical, immunological and pathological alterations. Ann. Clin. Pathol. 6:1130.
Ndelekwute, E. K., E. D. Assam, & E. M. Assam. 2018. Apparent nutrient digestibility, gut pH and digesta viscosity of broiler chickens fed acidified water. MOJ Anat. Physiol. 5:250-253. https://doi.org/10.15406/mojap.2018.05.00203
Nkukwana, T. T., V. Muchenje, P. J. Masika, & B. Mushonga. 2015. Intestinal morphology, digestive organ size and digesta pH of broiler chickens fed diets supplemented with or without Moringa oleifera leaf meal. S. Afr. J. Anim. Sci. 45:362-370. https://doi.org/10.4314/sajas.v45i4.2
Pop, L. M., L. C. Ştefănuţ, A. F. Tăbăran, A. L. Paştiu, Z. Kalmár, C. A. Magdaş, V. Mircean, & A. Györke. 2017. Influence of dietary artemisinin supplementation on productive performance and haematological parameters of broiler chickens. R. Bras. Zootec. 46:130-137. https://doi.org/10.1590/s1806-92902017000200008
Pratama, A. R., I. Mareta, T. Yudiarti, H. I. Wahyuni, E. Widiastuti, & S. Sugiharto. 2021. Administration of fermented Averrhoa bilimbi L. fruit filtrate through drinking water on growth performance, haematological indices, intestinal ecology and carcass characteristics of broiler chickens. Trop. Anim. Sci. J. 44:79-89. https://doi.org/10.5398/tasj.2021.44.1.79
Richardson, S. L., A. Hulikova, M. Proven, R. Hipkiss, M. Akannic, N. B. A. Roy, & P. Swietach. 2020. Single-cell o2 exchange imaging shows that cytoplasmic diffusion is a dominant barrier to efficient gas transport in red blood cells. Proc. Natl. Acad. Sci. 117:10067-10078. https://doi.org/10.1073/pnas.1916641117
Ruangpanit, Y., K. Matsushita, K. Mukai, & M. Kikusato. 2020. Effect of trehalose supplementation on growth performance and intestinal morphology in broiler chickens. Vet. Anim. Sci. 10:100142. https://doi.org/10.1016/j.vas.2020.100142
Salami, S. A., E. A. Agbonlahor, A. O. Salako, B. A. Sideeq, J. O. Agboola, & J. O. Atteh. 2018. Nutritive values of wheat bran-based broiler diet supplemented with different classes of enzymes. Trop. Agric. 95:246-256.
Sapsuha, Y., E. Suprijatna, S. Kismiati, & S. Sugiharto. 2021. Combination of probiotic and phythobiotic as an alternative for antibiotic growth promoter for broilers chickens-a review. Livest. Res. Rural Dev. 33:1-8.
Scarth, L. L. 2006. The Merck Veterinary Manual Online (8th edition). Reference Reviews 20:40-40. https://doi.org/10.1108/09504120610647492
Shakouri, M. D., P. A. Iji, L. L. Mikkelsen, & A. J. Cowieson. 2009. Intestinal function and gut microflora of broiler chickens as influenced by cereal grains and microbial enzyme supplementation. J. Anim. Physiol. Anim. Nutr. (Berl). 93:647-658. https://doi.org/10.1111/j.1439-0396.2008.00852.x
Shang, Q. H., S. J. Liu, T. F. He, H. S. Liu, S. Mahfuz, X. K. Ma, & X. S. Piao. 2020a. Effects of wheat bran in comparison to antibiotics on growth performance, intestinal immunity, barrier function, and microbial composition in broiler chickens. Poult. Sci. 99:4929-4938. https://doi.org/10.1016/j.psj.2020.06.031
Shang, Q., D. Wu, H. Liu, S. Mahfuz, & X. Piao. 2020b. The impact of wheat bran on the morphology and physiology of the gastrointestinal tract in broiler chickens. Animals 10:1831. https://doi.org/10.3390/ani10101831
SNI (Indonesian National Standard). 2015. Standard for broiler feed (SNI 8173.2:2015 and SNI 8173.3:2015). National Standardization Agency of Indonesia, Jakarta, Indonesia.
Stier, A., P. Bize, Q. Schull, J. Zoll, F. Singh, B. Geny, F. Gros, C. Royer, S. Massemin, & F. Criscuolo. 2013. Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front. Zool. 10:33. https://doi.org/10.1186/1742-9994-10-33
Sugiharto, S. 2016. Role of nutraceuticals in gut health and growth performance of poultry. J. Saudi Soc. Agric. Sci. 15:99-111. https://doi.org/10.1016/j.jssas.2014.06.001
Sugiharto, S. 2020. The potentials of two underutilized acidic fruits (Averrhoa bilimbi L. and Phyllanthus acidus L.) as phytobiotics for broiler chickens. J. Adv. Vet. Res. 10:179-185. https://advetresearch.com/index.php/AVR/article/view/464
Sugiharto, S. & S. Ranjitkar. 2019. Recent advances in fermented feed toward improved broiler chicken performance, gastrointestinal tract microecology and immune response: a review. Anim. Nut. 5:1-10. https://doi.org/10.1016/j.aninu.2018.11.001
Sugiharto, S., E. Widiastuti, I. Isroli, T. Yudiarti, T. A. Sartono, & H. I. Wahyuni. 2020. Effect of feeding fermented mixture of cassava pulp and Moringa oleifera leaf meal on immune responses, antioxidative status, biochemistry indices, and intestinal ecology of broilers. Vet. World. 13:392-399. https://doi.org/10.14202/vetworld.2020.392-399
Sugiharto, S., E. Widiastuti, A. R. Pratama, H. I. Wahyuni, T. Yudiarti, & T. A. Sartono. 2021. Hematological and intestinal responses of broilers to dietary supplementations of lactic fermented turmeric, black pepper or a mixture of both. Acta Univ. Agric. et Silvic. Mendelianae Brun. 69:101-110. https://doi.org/10.11118/actaun.2021.011
Sugiharto, S., T. Yudiarti, I. Isroli, & E. Widiastuti. 2018. Effect of feeding duration of Spirulina platensis on growth performance, haematological parameters, intestinal microbial population and carcass traits of broiler chicks. S. Afr. J. Anim. Sci. 48:98-108. https://doi.org/10.4314/sajas.v48i1.12
Taherpour, K., H. Moravej, M. Shivazad, M. Adibmoradi, & B. Yakhchali. 2009. Effects of dietary probiotic, prebiotic and butyric acid glycerides on performance and serum composition in broiler chickens. Afr. J. Biotechnol. 8:2329-2334. https://doi.org/10.5897/AJB09.178
Tufarelli, V., P. Baghban-Kanani, S. Azimi-Youvalari, B. Hosseintabar-Ghasemabad, M. Slozhenkina, I. Gorlov, A. Seidavi, T. Ayaşan, & V. Laudadio. 2021. Effects of horsetail (Equisetum arvense) and spirulina (Spirulina platensis) dietary supplementation on laying hens productivity and oxidative status. Animals. 11:335. https://doi.org/10.3390/ani11020335
Tunc, M. A., S. Yildirim, & M. A. Yorük. 2019. Effects of tarragon (Artemisia dracunculus) powder on broiler performance parameters and histopathology of internal organs. Austral. J. Vet. Sci. 51:113-118. https://doi.org/10.4067/S0719-81322019000300113
Utama, C. S., Z. Zuprizal, C. Hanim, & W. Wihandoyo. 2019. Effect of heating time on the chemical quality of wheat pollard as a prebiotic potential agent. Jurnal Aplikasi Teknologi Pangan 8:113-122. (full article in Indonesian language). https://doi.org/10.17728/jatp.5262
van Boven, M., A. Bouma, T. H. F. Fabri, E. Katsma, L. Hartog, G. Koch. 2008. Herd immunity to Newcastle disease virus in poultry by vaccination. Avian Pathol. 37:1-5. https://doi.org/10.1080/03079450701772391
Verruck, S. & E. S. Prudencio. 2019. Survival of Bifidobacterium ssp. during gastrointestinal passage and their mechanism of action for pathogenic bacteria inhibition in the gut: A concise review. Food Biol. 8:1-6. https://doi.org/10.25081/fb.2019.v8.3856
Vesa, T., P. Pochart, & P. Marteau. 2000. Pharmacokinetics of Lactobacillus plantarum NCIMB 8826, Lactobacillus fermentum KLD, and Lactococcus lactis MG 1363 in the human gastrointestinal tract. Aliment. Pharmacol. Ther. 14:823-828. https://doi.org/10.1046/j.1365-2036.2000.00763.x.
Villegas, P. 1987. Avian Virus Diseases Laboratory Manual. College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA.
Zhou, K., L. Su, & L. L. Yu. 2004. Phytochemicals and antioxidant properties in wheat bran. J. Agric. Food Chem. 52:6108-6114. https://doi.org/10.1021/jf049214g
Abudabos, A. M., A. H. Alyemni, Y. M. Dafalla, & R. U. Khan. 2017. The effect of phytogenics on growth traits, blood biochemical and intestinal histology in broiler chickens exposed to Clostridium perfringens challenge. J. Appl. Anim. Res. 46:691-695. https://doi.org/10.1080/09712119.2017.1383258
Aka-Tanimo, H. A., D. O. Oshibanjo, V. O. Adelowo, M. A. Akwashiki, I. W. Azi, O. C. James, S. Haruna, & A. Y. Sunday. 2020. Growth performance, carcass characteristics and hematology indices of broiler chicken fed graded levels of (Mangifera indica) mango leaf meal. Asian J. Res. Anim. Vet. Sci. 6:20-27.
Akhtar, M., M. M. Awais, M. I. Anwar, S. Ehtisham-ulHaque, A. Nasir, M. K. Saleemi, & K. Ashraf. 2015. The effect of infection with mixed Eimeria species on hematology and immune responses following Newcastle disease and infectious bursal disease booster vaccination in broilers. Vet. Q. 35:21-26. https://doi.org/10.1080/01652176.2014.991048
Alaqil, A. A., A. O. Abbas, H. S. El-Beltagi, H. El-Atty, K. Abd, G. M. Mehaisen, & E. S. Moustafa. 2020. Dietary supplementation of probiotic Lactobacillus acidophilus modulates cholesterol levels, immune response, and productive performance of laying hens. Animals 10:1588. https://doi.org/10.3390/ani10091588
Asheg, A., M. Levkut, V. Revajova, Z. Sevcikova, L. Kolodzieyski, & J. Pistl. 2002. T lymphocyte subpopulations and B lymphocyte cells in caecum and spleen of chicks infected with Salmonella enteritidis. Acta Histochem. 104:435-439. https://doi.org/10.1078/0065-1281-00666
Awad, W. A., K. Ghareeb, S. Abdel-Raheem, & J. Böhm, J. 2009. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult. Sci. 88:49-56. https://doi.org/10.3382/ps.2008-00244
Bolton, W. 1967. Poultry Nutrition. MAFF Bulletin No.174. HMSO, London.
Cimrin, T., R. I. Tunca, M. D. Avsaroglu, T. Ayasan, & S. Kücükersan. 2020. Effects of an antibiotic and two phytogenic substances (cinnamaldehyde and 1,8-cineole) on yolk fatty acid profile and storage period-associated egg lipid peroxidation level. R. Bras. Zootec. 49:e20190270. https://doi.org/10.37496/rbz4920190270
Del Vesco, A. P., E. Gasparino, D. O. Grieser, V. Zancanela, D. M. Voltolini, A. S. Khatlab, S. E. F. Guimarães, M. A. M. Soares, & A. R. O. Neto. 2015. Effects of methionine supplementation on the expression of protein deposition-related genes in acute heat stress-exposed broilers. PLoS ONE 10:e0115821. https://doi.org/10.1371/journal.pone.0115821.t002
Elghandour, M. M. Y., Z. L. Tan, S. H. Abu Hafsa, M. J. Adegbeye, R. Greiner, E. A. Ugbogu, J. C. Monroy, & A. Z. M. Salem. 2019. Saccharomyces cerevisiae as a probiotic feed additive to non and pseudo‐ruminant feeding: A review. J Appl. Microbiol. 128:658-674. https://doi.org/10.1111/jam.14416
Feng, Y., L. Wang, A. Khan, R. Zhao, S. Wei, & X. Jing. 2020. Fermented wheat bran by xylanase-producing Bacillus cereus boosts the intestinal microflora of broiler chickens. Poult. Sci. 99:263-271. https://doi.org/10.3382/ps/pez482
Fumagalli, S., F. Fattirolli, L. Guarducci, T. Cellai, S. Baldasseroni, F. Tarantini, D. Di Bari, G. Masotti, & N. Marchionni. 2011. Coenzyme Q10 terclatrate and creatine in chronic heart failure: a randomized, placebo-controlled, double-blind study. Clin. Cardiol. 34:211-7. https://doi.org/10.1002/clc.20846
Gunenc, A., C. Alswiti, & F. Hosseinian. 2017. Wheat bran as a prebiotic source and antioxidant activities of fiber fractions. J. Food Res. 6:1-10. https://doi.org/10.5539/jfr.v6n2p1
He, T., S. Mahfuz, X. Piao, D. Wu, W. Wang, H. Yan, T. Ouyang, & Y. Liu. 2021. Effects of live yeast (Saccharomyces cerevisiae) as a substitute to antibiotic on growth performance, immune function, serum biochemical parameters and intestinal morphology of broilers. J. Appl. Anim. Res. 49:15-22. https://doi.org/10.1080/09712119.2021.1876705
Helal, F., A. El-Badawi, S. El-Naggar, M. Shourrap, O. Aboelazab, & S. A. Hafsa. 2021. Probiotics role of Saccharomyces cerevisiae and Bacillus subtilis in improving the health status of rabbits’ gastrointestinal tract. Bull. Natl. Res. Cent. 45:1-9. https://doi.org/10.1186/s42269-021-00522-0
Hidanah, S., E. K. Sabdoningrum, R. S. Wahjuni, & S. Chusniati. 2018. Effects of meniran (Phyllanthus niruri L.) administration on leukocyte profile of broiler chickens infected with Mycoplasma gallisepticum. Vet. World. 11:834-839. https://doi.org/10.14202/vetworld.2018.834-839
Józefiak, D., S. Kaczmarek, & A. Rutkowski. 2008. A note on the effects of selected prebiotics on the performance and ileal microbiota of broiler chickens. J. Anim. Feed Sci. 17:392-397. https://doi.org/10.22358/jafs/66633/2008
Kırkpınar, F., Z. Açıkgöz, S. Mert, & O. Işık. 2018. Effects of dietary probiotic, prebiotic and enzyme mixture supplementation on performance, carcass, organ, ileal pH and viscosity of broilers. J. Anim. Prod. 59:1-9. https://doi.org/10.29185/hayuretim.469862
Konjufca, V. H., G. M. Pesti, & R. B. Bakalli. 1997. Modulation of cholesterol levels in broiler meat by dietary garlic and copper. Poult. Sci. 76:1264-1271. https://doi.org/10.1093/ps/76.9.1264
Kostadinović, L. M., S. T. Pavkov, J. D. Lević, T. A. GalonjaCoghill, G. K. Dozet, & N. C. Bojat. 2011. Effect of sulphachloropyrazine on antioxidative systems in blood and liver of broilers. Acta Vet. Brno. 80:165-170. https://doi.org/10.2754/avb201180020165
Lan, R. X., S. Q. Li, Z. Zhao, & L. L. An. 2020. Sodium butyrate as an effective feed additive to improve growth performance and gastrointestinal development in broilers. Vet. Med. Sci. 6:491-499. https://doi.org/10.1002/vms3.250
Li, B., J. Leblois, B. Taminiau, M. Schroyen, Y. Beckers, J. Bindelle, & N. Everaert. 2018. The effect of inulin and wheat bran on intestinal health and microbiota in the early life of broiler chickens. Poult. Sci. 97:3156-3165. https://doi.org/10.3382/ps/pey195
Lin, W. C. & T. T. Lee. 2020. Laetiporus sulphureus-fermented wheat bran enhanced the broiler growth performance by improving the intestinal microflora and inflammation status. Poult. Sci. 99:3606-3616. https://doi.org/10.1016/j.psj.2020.04.011
Mareta, I., G. Nathaniel, T. Yudiarti, E. Widiastuti, H. I. Wahyuni, & S. Sugiharto. 2020. Effect of Averrhoa bilimbi fruit filtrate and shrimp paste mixture on performance, gut microbes and blood profile of broilers. Indonesian Journal of Animal and Veterinary Science 25:182-189. https://doi.org/10.14334/jitv.v25i4.2515
Morales-López, S., J. A. Yepes, J. C. Prada-Herrera, & A. Torres-Jiménez. 2019. Enterobacteria in the 21st century: a review focused on taxonomic changes. J. Infect. Dev. Ctries. 13:265-273. https://doi.org/10.3855/jidc.11216
Müller, M., G. D. A. Hermes, C. E. Emanuel, J. J. Holst, E. G. Zoetendal, H. Smidt, F. Troost, F. G. Schaap, S. O. Damink, J. W. E. Jocken, K. Lenaerts, A. A. M. Masclee, & E. E. Blaak. 2020. Effect of wheat bran derived prebiotic supplementation on gastrointestinal transit, gut microbiota, and metabolic health: a randomized controlled trial in healthy adults with a slow gut transit. Gut Microbes 12:1704141. https://doi.org/10.1080/19490976.2019.1704141
Nasr El-Deen, N. A. M., S. A. M. El-Mandrawy, & M. A. Mahmoud. 2018. Trial in using Clostridium butyricum as prophylactic for Salmonellosis in broiler chicken: Hemato-biochemical, immunological and pathological alterations. Ann. Clin. Pathol. 6:1130.
Ndelekwute, E. K., E. D. Assam, & E. M. Assam. 2018. Apparent nutrient digestibility, gut pH and digesta viscosity of broiler chickens fed acidified water. MOJ Anat. Physiol. 5:250-253. https://doi.org/10.15406/mojap.2018.05.00203
Nkukwana, T. T., V. Muchenje, P. J. Masika, & B. Mushonga. 2015. Intestinal morphology, digestive organ size and digesta pH of broiler chickens fed diets supplemented with or without Moringa oleifera leaf meal. S. Afr. J. Anim. Sci. 45:362-370. https://doi.org/10.4314/sajas.v45i4.2
Pop, L. M., L. C. Ştefănuţ, A. F. Tăbăran, A. L. Paştiu, Z. Kalmár, C. A. Magdaş, V. Mircean, & A. Györke. 2017. Influence of dietary artemisinin supplementation on productive performance and haematological parameters of broiler chickens. R. Bras. Zootec. 46:130-137. https://doi.org/10.1590/s1806-92902017000200008
Pratama, A. R., I. Mareta, T. Yudiarti, H. I. Wahyuni, E. Widiastuti, & S. Sugiharto. 2021. Administration of fermented Averrhoa bilimbi L. fruit filtrate through drinking water on growth performance, haematological indices, intestinal ecology and carcass characteristics of broiler chickens. Trop. Anim. Sci. J. 44:79-89. https://doi.org/10.5398/tasj.2021.44.1.79
Richardson, S. L., A. Hulikova, M. Proven, R. Hipkiss, M. Akannic, N. B. A. Roy, & P. Swietach. 2020. Single-cell o2 exchange imaging shows that cytoplasmic diffusion is a dominant barrier to efficient gas transport in red blood cells. Proc. Natl. Acad. Sci. 117:10067-10078. https://doi.org/10.1073/pnas.1916641117
Ruangpanit, Y., K. Matsushita, K. Mukai, & M. Kikusato. 2020. Effect of trehalose supplementation on growth performance and intestinal morphology in broiler chickens. Vet. Anim. Sci. 10:100142. https://doi.org/10.1016/j.vas.2020.100142
Salami, S. A., E. A. Agbonlahor, A. O. Salako, B. A. Sideeq, J. O. Agboola, & J. O. Atteh. 2018. Nutritive values of wheat bran-based broiler diet supplemented with different classes of enzymes. Trop. Agric. 95:246-256.
Sapsuha, Y., E. Suprijatna, S. Kismiati, & S. Sugiharto. 2021. Combination of probiotic and phythobiotic as an alternative for antibiotic growth promoter for broilers chickens-a review. Livest. Res. Rural Dev. 33:1-8.
Scarth, L. L. 2006. The Merck Veterinary Manual Online (8th edition). Reference Reviews 20:40-40. https://doi.org/10.1108/09504120610647492
Shakouri, M. D., P. A. Iji, L. L. Mikkelsen, & A. J. Cowieson. 2009. Intestinal function and gut microflora of broiler chickens as influenced by cereal grains and microbial enzyme supplementation. J. Anim. Physiol. Anim. Nutr. (Berl). 93:647-658. https://doi.org/10.1111/j.1439-0396.2008.00852.x
Shang, Q. H., S. J. Liu, T. F. He, H. S. Liu, S. Mahfuz, X. K. Ma, & X. S. Piao. 2020a. Effects of wheat bran in comparison to antibiotics on growth performance, intestinal immunity, barrier function, and microbial composition in broiler chickens. Poult. Sci. 99:4929-4938. https://doi.org/10.1016/j.psj.2020.06.031
Shang, Q., D. Wu, H. Liu, S. Mahfuz, & X. Piao. 2020b. The impact of wheat bran on the morphology and physiology of the gastrointestinal tract in broiler chickens. Animals 10:1831. https://doi.org/10.3390/ani10101831
SNI (Indonesian National Standard). 2015. Standard for broiler feed (SNI 8173.2:2015 and SNI 8173.3:2015). National Standardization Agency of Indonesia, Jakarta, Indonesia.
Stier, A., P. Bize, Q. Schull, J. Zoll, F. Singh, B. Geny, F. Gros, C. Royer, S. Massemin, & F. Criscuolo. 2013. Avian erythrocytes have functional mitochondria, opening novel perspectives for birds as animal models in the study of ageing. Front. Zool. 10:33. https://doi.org/10.1186/1742-9994-10-33
Sugiharto, S. 2016. Role of nutraceuticals in gut health and growth performance of poultry. J. Saudi Soc. Agric. Sci. 15:99-111. https://doi.org/10.1016/j.jssas.2014.06.001
Sugiharto, S. 2020. The potentials of two underutilized acidic fruits (Averrhoa bilimbi L. and Phyllanthus acidus L.) as phytobiotics for broiler chickens. J. Adv. Vet. Res. 10:179-185. https://advetresearch.com/index.php/AVR/article/view/464
Sugiharto, S. & S. Ranjitkar. 2019. Recent advances in fermented feed toward improved broiler chicken performance, gastrointestinal tract microecology and immune response: a review. Anim. Nut. 5:1-10. https://doi.org/10.1016/j.aninu.2018.11.001
Sugiharto, S., E. Widiastuti, I. Isroli, T. Yudiarti, T. A. Sartono, & H. I. Wahyuni. 2020. Effect of feeding fermented mixture of cassava pulp and Moringa oleifera leaf meal on immune responses, antioxidative status, biochemistry indices, and intestinal ecology of broilers. Vet. World. 13:392-399. https://doi.org/10.14202/vetworld.2020.392-399
Sugiharto, S., E. Widiastuti, A. R. Pratama, H. I. Wahyuni, T. Yudiarti, & T. A. Sartono. 2021. Hematological and intestinal responses of broilers to dietary supplementations of lactic fermented turmeric, black pepper or a mixture of both. Acta Univ. Agric. et Silvic. Mendelianae Brun. 69:101-110. https://doi.org/10.11118/actaun.2021.011
Sugiharto, S., T. Yudiarti, I. Isroli, & E. Widiastuti. 2018. Effect of feeding duration of Spirulina platensis on growth performance, haematological parameters, intestinal microbial population and carcass traits of broiler chicks. S. Afr. J. Anim. Sci. 48:98-108. https://doi.org/10.4314/sajas.v48i1.12
Taherpour, K., H. Moravej, M. Shivazad, M. Adibmoradi, & B. Yakhchali. 2009. Effects of dietary probiotic, prebiotic and butyric acid glycerides on performance and serum composition in broiler chickens. Afr. J. Biotechnol. 8:2329-2334. https://doi.org/10.5897/AJB09.178
Tufarelli, V., P. Baghban-Kanani, S. Azimi-Youvalari, B. Hosseintabar-Ghasemabad, M. Slozhenkina, I. Gorlov, A. Seidavi, T. Ayaşan, & V. Laudadio. 2021. Effects of horsetail (Equisetum arvense) and spirulina (Spirulina platensis) dietary supplementation on laying hens productivity and oxidative status. Animals. 11:335. https://doi.org/10.3390/ani11020335
Tunc, M. A., S. Yildirim, & M. A. Yorük. 2019. Effects of tarragon (Artemisia dracunculus) powder on broiler performance parameters and histopathology of internal organs. Austral. J. Vet. Sci. 51:113-118. https://doi.org/10.4067/S0719-81322019000300113
Utama, C. S., Z. Zuprizal, C. Hanim, & W. Wihandoyo. 2019. Effect of heating time on the chemical quality of wheat pollard as a prebiotic potential agent. Jurnal Aplikasi Teknologi Pangan 8:113-122. (full article in Indonesian language). https://doi.org/10.17728/jatp.5262
van Boven, M., A. Bouma, T. H. F. Fabri, E. Katsma, L. Hartog, G. Koch. 2008. Herd immunity to Newcastle disease virus in poultry by vaccination. Avian Pathol. 37:1-5. https://doi.org/10.1080/03079450701772391
Verruck, S. & E. S. Prudencio. 2019. Survival of Bifidobacterium ssp. during gastrointestinal passage and their mechanism of action for pathogenic bacteria inhibition in the gut: A concise review. Food Biol. 8:1-6. https://doi.org/10.25081/fb.2019.v8.3856
Vesa, T., P. Pochart, & P. Marteau. 2000. Pharmacokinetics of Lactobacillus plantarum NCIMB 8826, Lactobacillus fermentum KLD, and Lactococcus lactis MG 1363 in the human gastrointestinal tract. Aliment. Pharmacol. Ther. 14:823-828. https://doi.org/10.1046/j.1365-2036.2000.00763.x.
Villegas, P. 1987. Avian Virus Diseases Laboratory Manual. College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA.
Zhou, K., L. Su, & L. L. Yu. 2004. Phytochemicals and antioxidant properties in wheat bran. J. Agric. Food Chem. 52:6108-6114. https://doi.org/10.1021/jf049214g
Authors
PratamaA., YudiartiT., SugihartoS., & AyaşanT. (2022). Blood and Intestine Profile of Broilers Fed Averrhoa bilimbi Fruit, Wheat Bran, and Yeast Blends. Tropical Animal Science Journal, 45(1), 44-55. https://doi.org/10.5398/tasj.2022.45.1.44
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