Growth, Blood, and Intestinal Indices of Broilers at High Density Pens Provided with Fermented Averrhoa bilimbi Fruit Filtrate

S. Sugiharto, E. Widiastuti, T. Sartono, H. Wahyuni, A. Pratama, T. Yudiarti


The present study investigated the effect of fermented Averrhoa bilimbi fruit filtrate (FABFF) on growth, blood indices, and gut ecology of broilers raised at a high stocking density. Using 378 chicks (14 days of age), the study was arranged based on a factorial design with stocking densities (normal with 9 birds/m2 or high with 18 birds/m2) and treatment with 2% FABFF from drinking water or not as the two factors. Live body weight and feed consumption were registered weekly, while blood and intestinal contents were collected at day 35. Broilers at high density receiving FABFF had the lowest (p<0.05) feed conversion ratio (FCR). Thymus was smaller (p<0.05) in high-stocked broilers receiving only drinking water. Birds administered FABFF had greater (p<0.05) bursa of Fabricius than birds given plain water. The FABFF elevated (p<0.05) serum superoxide dismutase (SOD) levels of broilers. The malondialdehyde levels were higher (p<0.05) in high-stocked broilers given drinking water compared to normal-stocked broilers given drinking water or high-stocked broilers receiving FABFF. Drinking FABFF elevated (p<0.05) the ratio of lactic acid bacteria/coliform in the ileum. Cecal coliform was less (p<0.05) in chicks receiving FABFF than those receiving only water. High-stocked broilers receiving FABFF showed lower (p<0.05) Enterobacteriaceae counts than the other birds. The ratio of lactic acid bacteria/coliform increased (p<0.05) in broilers receiving FABFF. In conclusion, FABFF was capable of maintaining the development of immune organs and improving FCR, antioxidative status, and intestinal microbial balance of broilers stocked at high-density pens.


Abo Ghanima, M. M., M. E. Abd El-Hack, A. E. Taha, V. Tufarelli, V. Laudadio, & M. A. E. Naiel. 2020. Assessment of stocking rate and housing system on performance, carcass traits, blood indices, and meat quality of french pekin ducks. Agriculture 10:273.
Abudabos, A. M., M. A. Murshed, M. M. Qaid, & A. G. Abdelrahman. 2016. Effect of probiotics on serum biochemical and blood constituents in chicken challenged with Salmonella enterica Subsp Typhimurium. Trop. J. Pharm. Res. 15:461.
Adeyemi, O. A., E. O. Adedoyin, O. O. Olaleye, P. C. Njoku, & K. A. Sanwo. 2015. Effects of ascorbic acid supplementation on broiler chickens stocked at two different densities in a humid tropical environment. Mal. J. Anim. Sci. 18:89-101.
Agusetyaningsih, I., E. Widiastuti, H. I. Wahyuni, T. Yudiarti, R. Murwani, T. A. Sartono, & S. Sugiharto. 2021. Effect of encapsulated Cosmos caudatus leaf extract on the physiological conditions, immune competency, and antioxidative status of broilers at high stocking density. Annals Animal of Science
Alkhalf, A., M. Alhaj, & I. Al-Homidan. 2010. Influence of probiotic supplementation on immune response of broiler chicks. Egypt. Poult. Sci. 30:271-280.
Altaf, M. T., A. Mahmud, S. Mehmood, & Saima. 2019. Effects of supplemented growth promoters on performance and intestinal morphology in broilers reared under different stocking densities. Rev. Bras. Cienc. Avic. 21:eRBCA-2019-1073.
Amalia, U., Sumardianto, & T. W. Agustini. 2018. Characterization of lactic acid bacteria (LAB) isolated from Indonesian shrimp paste (terasi). IOP. Conf. Ser. Earth. Environ. Sci. 116:012049.
Bai, K., C. Feng, L. Jiang, L. Zhang, J. Zhang, L. Zhang, & T. Wang. 2018. Dietary effects of Bacillus subtilis fmbj on growth performance, small intestinal morphology, and its antioxidant capacity of broilers. Poult. Sci. 97:2312-2321.
Beg, M. A. H., M. A. Baqui, N. R. Sarker, & M. M. Hossain. 2011. Effect of stocking density and feeding regime on performance of broiler chicken in summer season. Int. J. Poult. Sci. 10:365-375.
Bolton, W. 1967. Poultry Nutrition. MAFF Bulletin No.174. HMSO, London.
Cengiz, O., B. H. Koksal, O. Tatli, O. Sevim, H. Avci, T. Epikmen, D. Beyaz, S. Buyukyoruk, M. Boyacioglu, A. Uner, & A. G. Onol. 2012. Influence of dietary organic acid blend supplementation and interaction with delayed feed access after hatch on broiler growth performance and intestinal health. Vet. Med. (Praha). 57:515–528.
Chegini, S., A. Kiani, B. P. Kavan, & H. Rokni. 2019. Effects of propolis and stocking density on growth performance, nutrient digestibility, and immune system of heat-stressed broilers. Ital. J. Anim. Sci. 18:868-876.
Chen, Y., Y. Chen, H. Zhang, & T. Wang. 2020. Pterostilbene as a protective antioxidant attenuates diquat-induced liver injury and oxidative stress in 21-day-old broiler chickens. Poult. Sci. 99:3158-3167.
Dell’Anno, M., M. L. Callegari, S. Reggi, V. Caprarulo, C. Giromini, A. Spalletta, S. Coranelli, C. A. S. Rossi, & L. Rossi. 2021. Lactobacillus plantarum and Lactobacillus reuteri as functional feed additives to prevent diarrhoea in weaned piglets. Animals 11:1766.
Delles, R. M., Y. L. Xiong, A. D. True, T. Ao, & K. A. Dawson. 2014. Dietary antioxidant supplementation enhances lipid and protein oxidative stability of chicken broiler meat through promotion of antioxidant enzyme activity. Poult. Sci. 93:1561-70.
Fascina, V. B., G. A. M. Pasquali, F. B. Carvalho, E. M. Muro, F. Vercese, M. M. Aoyagi, A. C. Pezzato, E. Gonzales, & J. R. Sartori. 2017. Effects of phytogenic additives and organic acids, alone or in combination, on the performance, intestinal quality and immune responses of broiler chickens. Rev. Bras. Cienc. Avic. 19:497-508.
Ghazalah, I., A. M. Attal, K. M. outElkloub, R. El moustafa, & F. H. Shata. 2011. Effect of supplementation of organic acids on performance, nutrients digestibility and health of broiler chicks. Int. J. Poult. Sci. 10:176-184.
Gholami, M., M. Chamani, A. Seidavi, A. A. Sadeghi, & M. Aminafschar. 2020. Effects of stocking density and climate region on performance, immunity, carcass characteristics, blood constitutes, and economical parameters of broiler chickens. Revista Brasileira de Zootecnia 49:e20190049.
Haque, M. H., S. Sarker, M. S. Islam, M. A. Islam, M. R. Karim, M. Kayesh, M. Shiddiky, & M. S. Anwer. 2020. Sustainable antibiotic-free broiler meat production: current trends, challenges, and possibilities in a developing country perspective. Biology 9:411.
He, S., Q. Yin, Y. Xiong, D. Liu, & H. Hu. 2020. Effects of dietary fumaric acid on the growth performance, immune response, relative weight and antioxidant status of immune organs in broilers exposed to chronic heat stress. Czech. J. Anim. Sci. 65:104-113.
Hornsey, V. S., K. McColl, O. Drummond, L. McMillan, A. Morrison, L. Morrison, I. R. MacGregor, & C. V. Prowse. 2006. Extended storage of platelets in SSP platelet additive solution. Vox. Sang. 91:41-6.
Jang, I.-S., S.-H. Yun, Y.-H. Ko, S.-Y. Kim, M.-H. Song, J.-S. Kim, S.-H. Sohn, & Y.-S. Moon. 2014. The effect of stocking density and strain on the performance and physiological adaptive responses in broiler chickens. Korean Journal of Poultry Science 41:205-15.
Kobayashi, T., M. Kajiwara, M. Wahyuni, T. Kitakado, N. HamadaSato, C. Imada, & E. Watanabe. 2003. Isolation and characterization of halophilic lactic acid bacteria isolated from “terasi” shrimp paste: A traditional fermented seafood product in Indonesia. J. Gen. Appl. Microbiol. 49:279-286.
Law, F. L., I. Zulkifli, A. F. Soleimani, J. B. Liang, & E. A. Awad. 2019. Effects of reduced-protein diets supplemented with protease in broiler chickens under high stocking density. Anim. Prod. Sci. 59:2212-2221.
Li, W., F. Wei, B. Xu, Q. Sun, W. Deng, H. Ma, J. Bai, & S. Li. 2019. Effect of stocking density and alpha-lipoic acid on the growth performance, physiological and oxidative stress and immune response of broilers. Asian-Australas. J. Anim. Sci. 32:1914-1922.
Maeda, M., A. Shibata, G. Biswas, H. Korenaga, T. Kono, T. Itami, & M. Sakai. 2014. Isolation of lactic acid bacteria from Kuruma shrimp (Marsupenaeus japonicus) intestine and assessment of immunomodulatory role of a selected strain as probiotic. Mar. Biotechnol. 16:181-192.
Magnuson, A. D., G. Liu, T. Sun, S. A. Tolba, L. Xi, R. Whelan, & X. G. Lei. 2020. Supplemental methionine and stocking density affect antioxidant status, fatty acid profiles, and growth performance of broiler chickens. J. Anim. Sci. 98:skaa092.
Mahmoud, R. M. & T. K. El-Rayes. 2016. Effect of stocking density and probiotic supplementation on broiler performance. Journal of Animal and Poultry Production 7:491-497.
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. Jurnal Ilmu Ternak dan Veteriner 25:182-189.
Messaï, C. R., O. Salhi, D. Khelef, A. Lounas, A. Mohamed-Cherif, R. Kaidi, & K. Aït-Oudhia. 2019. Serological, clinical, and risk factors of the Newcastle disease on broilers flocks in Algeria. Vet. World. 12:938-944.
Nasri, H. & A. Baradaran. 2006. Platelet count and mean volume (MPV) in association with plasma HCO3 - in regular hemodialysis patients. Rev. Bras. Hematol. Hemoter. 28:127-130.
Park, B. S., K. H. Um, S. O. Park, & V. A. Zammit. 2018. Effect of stocking density on behavioral traits, blood biochemical parameters and immune responses in meat ducks exposed to heat stress. Arch. Anim. Breed. 61:425-432.
Patria, C. A., R. Afnan, & I. I. Arief. 2016. Physical and microbiological qualities of kampong-broiler crossbred chickens meat raised in different stocking densities. Med. Pet. 39:141-147.
Pearlin, B. V., S. Muthuvel, P. Govidasamy, M. Villavan, M. Alagawany, M. Ragab Farag, K. Dhama, & M. Gopi. 2020. Role of acidifiers in livestock nutrition and health: A review. J. Anim. Physiol. Anim. Nutr. (Berl). 104:558-569.
Peng, M., J. Han, L. Li, & H. Ma. 2016. Suppression of fat deposition in broiler chickens by (-)-hydroxycitric acid supplementation: a proteomics perspective. Sci. Rep. 6:32580.
Pratama, A., I. Mareta, T. Yudiarti, H. I. Wahyuni, E. Widiastuti, & S. Sugiharto. 2021. Administration of fermented Averrhoa bilimbi L. fruit filtrate on growth, hematological, intestinal, and carcass indices of broilers. Trop. Anim. Sci. J. 44:79-89.
Qaid, M. M. & M. A. Al-Garadi. 2021. Protein and amino acid metabolism in poultry during and after heat stress: a review. Animals 11:1167.
Qaid, M., H. Albatshan, T. Shafey, E. Hussein, & A. M. Abudabos. 2016. Effect of stocking density on the performance and immunity of 1- to 14-d- old broiler chicks. Rev. Bras. Cienc. Avic. 18:683-692.
Rashidi, N., M. R. Ghorbani, A. Tatar, & S. Salari. 2019. Response of broiler chickens reared at high density to dietary supplementation with licorice extract and probiotic. J. Anim. Physiol. Anim. Nutr. (Berl). 103:100-107.
Salhi, O., C.-R. Messai, K. Ait-Oudhia, A. Lounas, A. Abdelli, R. Kaidi, & D. Khelef. 2020. Epidemiological, serological, clinical and risk factors of infectious bursal disease (IBD), in broilers flocks in Algeria. Agriculture 1-2:113-114.
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.
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.
Uzum, M. H., & H. D. O. Toplu. 2013. Effects of stocking density and feed restriction on performance, carcass, meat quality characteristics and some stress parameters in broilers under heat stress. Revue. Méd. Vét. (Toulouse). 164:546-554.
Wang, H., X. Ni, X. Qing, D. Zeng, M. Luo, L. Liu, G. Li, K. Pan, & B. Jing. 2017. Live probiotic Lactobacillus johnsonii BS15 promotes growth performance and lowers fat deposition by improving lipid metabolism, intestinal development, and gut microflora in broilers. Front. Microbiol. 8:1073.
Zaytsoff, S. J. M., C. L. J. Brown, T. Montina, G. A. S. Metz, D. W. Abbott, R. Richard, E. Uwiera & G. D. Inglis. 2019.  Corticosterone-mediated physiological stress modulates hepatic lipid metabolism, metabolite profiles, and systemic responses in chickens. Sci. Rep. 9:19225.


S. Sugiharto (Primary Contact)
E. Widiastuti
T. Sartono
H. Wahyuni
A. Pratama
T. Yudiarti
SugihartoS., WidiastutiE., SartonoT., WahyuniH., PratamaA., & YudiartiT. (2022). Growth, Blood, and Intestinal Indices of Broilers at High Density Pens Provided with Fermented Averrhoa bilimbi Fruit Filtrate. Tropical Animal Science Journal, 45(2), 202-212.

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