Administration of Fermented Averrhoa bilimbi L. Fruit Filtrate on Growth, Hematological, Intestinal, and Carcass Indices of Broilers

  • A. Pratama Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University
  • I. Mareta Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University
  • T. Yudiarti Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University
  • H. I. Wahyuni Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University
  • E. Widiastuti Department of Animal Science, Faculty of Animal and Agricultural Sciences, Diponegoro University
  • S. Sugiharto Faculty of Animal and Agricultural Sciences, Diponegoro University
Keywords: broiler, fermented fruit filtrate, lactic acid bacteria, organic acids


The study investigated the effects of administration of graded levels of fermented Averrhoa bilimbi L. fruit filtrate in drinking water on the growth performance, hematological variables, intestinal ecology, and carcass characteristics of broilers. The experiment was arranged based on a completely randomized design. Two hundred day-old-Lohmann broiler chicks were randomly assigned into 4 treatment groups, each consisting of 5 replications with 10 chicks in each replication. The treatments were administration of fermented A. bilimbi L. fruit filtrate through drinking water at concentrations of 0% (CONT), 0.5% (FAB05), 1.0% (FAB1), and 2.0% (FAB2). Blood was sampled on days 21 and 33, while intestinal segments and digesta were collected on day 33. Feed conversion ratio (FCR) was improved (p<0.05) with the increased concentrations of fermented filtrate in drinking water. Body weight, cumulative feed intake, and mortality of broilers were not affected by the treatments. On day 21, thrombocytes decreased (p<0.05) with the increased concentrations of fermented filtrate. On day 33, leukocytes and lymphocytes were lower (p<0.05) in treated chicks than in control. On day 21, the high-density lipoprotein (HDL) and aspartate aminotransferase (AST) increased (p<0.05) with the enhanced fermented filtrate concentrations. On day 33, creatinine and alanine aminotransferase (ALT) increased (p<0.05) following the increased fermented filtrate concentration in drinking water. Fermented fruit filtrate increased (p<0.05) jejunal villi height and ileal crypt depth. Fermented filtrate also resulted in higher (p<0.05) pH values of jejunum. The Enterobacteriaceae counts in the ileum decreased (p<0.05) with the increased fermented filtrate concentration in drinking water. Fermented fruit filtrate decreased (p<0.05) the liver and caeca weights and increased (p<0.05) the proventriculus weight. In conclusion, administration of 2% of fermented A. bilimbi L. fruit filtrate (pH 1.83) through drinking water improved FCR, physiological condition, and intestinal ecology of broilers. The addition of fermented fruit filtrate up to 2% in drinking water did not exert a negative effect on the carcass characteristics of broilers.


Download data is not yet available.


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.

Agboola, A. F., B. R. O. Omidiwura, O. Odu, I. O. Popoola, & E. A. Iyayi. 2015. Effects of organic acid and probiotic on performance and gut morphology in broiler chickens. S. Afr. J. Anim. Sci. 45:494-501.

Ahn, H. Y., M. Kim, J. S. Chae, Y. T. Ahn, J. H. Sim, I. D. Choi, & S. H. Lee. 2015. Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduces fasting triglycerides and enhances apolipoprotein A-V levels in non-diabetic subjects with hypertriglyceridemia. Atherosclerosis. 241:649-656.

Alhassan, A. M, & Q. U. Ahmed. 2016. Averrhoa bilimbi Linn.: A review of its ethnomedicinal uses, phytochemistry, and pharmacology. J. Pharm. Bioallied. Sci. 8:265-271. http://doi: 10.4103/0975-7406.199342.

Awad, A.W., K. Ghareeb., S. Abdel-Raheem, & J. Böhm. 2009. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult. Sci. 88:49-55.

Aziz, N. A. 2016. A review of the antimicrobial properties of three selected underutilized fruits of Malaysia. Int. J. Pharmaceutic. Clin. Res. 8:1278-1283.

Bai, S. P., A. M. Wu, X. M. Ding, Y. Lei, J. Bai, K. Y. Zhang, & J. S. Chio. 2013. Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poult. Sci. 92:663-670.

Bolton, W. 1967. MAFF Bulletin. No.174. Poultry Nutrition. HMSO, London.

Boroojeni F. G., W. Vahjen, A. Mader, F. Knorr, I. Ruhnke, I. Röhe, A. Hafeez, C. Villodre, K. Männer, & J. Zentek. 2014. The effects of different thermal treatments and organic acid levels in feed on microbial composition and activity in gastrointestinal tract of broilers. Poult. Sci. 93:1440-1452.

Brzósk, F., B. Śliwiński, & O. Michalik-Rutkowska. 2013. Effect of dietary acidifier on growth, mortality, post-slaughter parameters and meat composition of broiler chickens. Ann. Anim. Sci. 13:85-96.

Chowdhury, S. S., Md. Al-Amin, M. Jamila, S. Haque, T. Ahmed, & M. E. H. Mazumder. 2009. Infrared spectroscopic characterization, free radical scavenging and cytotoxic evaluation of chitosan extracted from Penaeus monodon shells. S. J. Pharm. Sci. 2: 27-30.

Fouladi, P., Y. Ebrahimnezhad, H. Aghdam Shahryar, N. Maheri, & A. Ahmadzadeh. 2018. Effects of organic acids supplement on performance, egg traits, blood serum biochemical parameters and gut microflora in female Japanese quail (Coturnix coturnix japonica). Rev. Bras. Cienc. Avic. 20:133-144.

Fazayeli-Rad, A. R., H. Nazarizadeh, M. Vakili & R. Nourmohammadi. 2014. Effect of citric acid on performance, nutrient retention and tissue biogenic amine contents in breast and thigh meat from broiler chickens. Europ. Poult. Sci. 78:1-9.

Ferdous, F., D. Maurice, & T. Scott. 2008. Broiler chick thrombocyte response to lipopolysaccharide. Poult. Sci. 87:61-63.

Forte, C., G. Acuti., E. Manuali., P. Casagrande-Proietti, S. Pavone, M. Trabalza-Marinucci, L. Moscati, A. Onofri, C. Lorenzetti, & M. P. Franciosini. 2016. Effects of two different probiotics on microflora, morphology, and morphometry of gut in organic laying hens. J. Poult. Sci. 95:2528–2535.

Gao, P., C. Ma, Z. Sun, L. Wang, S. Huang, X. Su, J. Xu, & H. Zhang. 2017. Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome. 5:91. https:/

Hedayati, M., M. Manafi, S. Khalaji, M. Yari, A. Esapour, E. Nazari, & F. Mohebi. 2015. Combination effect of probiotic and organic acids on blood biochemistry and immunity parameters of broiler. Int. J. Agric. Innov. Res. 3:1288-1293.

Herdian, H., L. Istiqomah, E. Damayanti, A.E. Suryani, A. S. Anggraeni, N. Rosyada, & A. Susilowati. 2018. Isolation of cellulolytic lactic-acid bacteria from mentok (Anas moschata) gastro-intestinal tract. Trop. Anim. Sci. J. 41:200-206.

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:/

Isroli, I., T. Yudiarti, E. Widiastuti, H. I. Wahyuni, T. A. Sartono, & S. Sugiharto. 2018. Effect of Bacillus probiotics on internal organs and carcass characteristics of broiler chicks infected with avian pathogenic Escherichia coli. Livest. Res. Rural Dev. 30:11.

Khan, S. H, & J. Iqbal. 2016. Recent advances in the role of organic acids in poultry nutrition. J. Appl. Anim. Res. 44:359-369.

Mabelebele, M., O. J. Alabi., J. W. Ngambi, D. Norris, & M. M. Ginindza. 2014. Comparison of gastrointestinal tracts and pH values of digestive organs of Ross 308 broiler and indigenous Venda chickens fed the same diet. Asian J. Anim. Vet. Adv. 9:71-76.

Ngasotter, S., D. Waikhom, S. Mukherjee, M. S. Devi, & A. S. Singh. 2020. Diversity of lactic acid bacteria (LAB) in fermented fish products: a review. Int. J. Curr. Microbiol. App. Sci. 9:2238-2249.

Nosrati, M., F. Javandel, L. M. Camacho, A. Khusro, M. Cipriano, A. Seidavi, & A. Z. M. Salem. 2019. The effects of antibiotic, probiotic, organic acid, vitamin C, and Echinacea purpurea extract on performance, carcass characteristics, blood chemistry, microbiota, and immunity of broiler chickens. J. Appl. Poult. Res. 26:295-306.

Nourmohammadi, R., & H. Khosravinia. 2015. Acidic stress caused by dietary administration of citric acid in broiler chickens. Arch. Anim. Breed. 58:309-315.

Olnood, C. G., S. M. Beski, P. A. Iji, & M. Choct. 2015. Delivery routes for probiotics: Effects on broiler performance, intestinal morphology and gut microflora. Anim. Nutr. 1:192-202.

Palamidi, I., & K. C. Mountzouris. 2018. Diet supplementation with an organic acids-based formulation affects gut microbiota and expression of gut barrier genes in broilers. Anim. Nut. 4:367-377.

Pearlin, B. V., S. Muthuvel, P. Govidasamy, M. Villavan, M. Alagawany, M. R. Farag, K. Dhama, & M. Gopi. 2020. Role of acidifiers in livestock nutrition and health: A review. J. Anim. Physiol. Anim. Nutr. 104:558-569.

Recoules, E., M. Lessire, V. Labas, M. J. Duclos, L. Combes-Soia, L. Lardic, C. Peyronnet, A. Quinsac, A. Narcy, & S. Réhault-Godbert. 2019. Digestion dynamics in broilers fed rapeseed meal. Sci. Rep. 9:3052.

Renatami, R. K., A. Noerdin, B. Irawan, & A. Soufya. 2018. Effects of differing concentrations of bilimbi (Averrhoa bilimbi L.) extract gel on enamel surface roughness. J. Phys. Conf. Ser. 1073:032012.

Rodjan, P., K. Soisuwan, K. Thongprajukaew, Y. Theapparat, S. Khongthong, J. Jeenkeawpieam, & T. Salaeharae. 2018. Effect of organic acids or probiotics alone or in combination on growth performance, nutrient digestibility, enzyme activities, intestinal morphology and gut microflora in broiler chickens. J. Anim. Physiol. Anim. Nutr. 102:931-940.

Rodríguez, L. G. R., F. Mohamed, J. Bleckwedel, R. Medina, L. De Vuyst, E. M. Hebert, & F. Mozzi. 2019. Diversity and functional properties of lactic acid bacteria isolated from wild fruits and flowers present in Northern Argentina. Front. Microbiol. 10:1091.

Sabour, S., S. A. Tabeidiana, & Sadeghi, G. 2019. Dietary organic acid and fiber sources affect performance, intestinal morphology, immune responses and gut microflora in broilers. Anim. Nut. 5:156-162.

Saki, A. A., S. M. Eftekhari, P. Zamani, H. Aliarabi, & M. Abbasinezhad. 2012. Effects of an organic acid mixture and methionine supplements on intestinal morphology, protein and nucleic acids content, microbial population and performance of broiler chickens. Anim. Prod. Sci. 51:1025-1033.

Sugiharto, S. 2016. Role of nutraceuticals in gut health and growth performance of poultry. J. Saudi Soc. Agric. Sci. 15: 99-111.

Sugiharto, S., T. Yudiarti, I. Isroli, E. Widiastuti, & E. Kusumanti. 2017. Dietary supplementation of probiotics in poultry exposed to heat stress - a review. Ann. Anim. Sci. 3:591-604.

Sugiharto, S., T. Yudiarti, I. Isroli, E. Widiastuti, H. I. Wahyuni, & T. A. Sartono. 2018. The effect of fungi-origin probiotic Chrysonilia crassa in comparison to selected commercially used feed additives on broiler chicken performance, intestinal microbiology, and blood indices. J. Adv. Vet. Anim. Res. 5:332-342.

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.

Sugiharto, S., T. Yudiarti, & I. Isroli. 2019. Growth performance, haematological parameters, intestinal microbiology, and carcass characteristics of broiler chickens fed two-stage fermented cassava pulp during finishing phase. Trop. Anim. Sci. J. 42:113-120.

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.

Widiastuti, E., I. Isroli, R. Murwani, T. A. Sartono, H. I. Wahyuni, T. Yudiarti, & S. Sugiharto. 2019. Dietary supplementation of butyric acid, probiotic Bacillus subtilis or their combination on weight gain, internal organ weight and carcass traits of the Indonesian indigenous crossbred chickens. Livest. Res. Rural Dev. 31:9.

Widyastuti, Y., Rohmatussolihat, & A. Febrisiantosa. 2014. The role of lactic acid bacteria in milk fermentation. Food Nutr. Sci. 5:435-442.

Wijayanti, D. A., O. Sjofjan, & I. H. Djunaidi. 2019. In vitro antimicrobial test for Averrhoa bilimbi extract at different level. Jurnal Ilmu-Ilmu Peternakan. 29:9-14.

Wiradimadja, R., W. D. Tanwiriah, & D. Rusmana. 2015. Effect of starfruit (Averrhoa bilimbi L.) giving in the diet on the performance, carcass and income over feed cost native chicken. J. Ziraa’ah. 40:86-91. (full article in Bahasa)

Wu, Z., H. Zhou, F. Li, N. Zhang, & Y. Zhu. 2019. Effect of dietary fiber levels on bacterial composition with age in the cecum of meat rabbits. Microbiol. Open. 8:5.

Xu, Z. R., C. H. Hu, M. S. Xia, X. A. Zhan, & M. Q. Wang. 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult. Sci. 82:1030-1036.

Yang, X., H. Xin, C. Yang, & X. Yang. 2018. Impact of essential oils and organic acids on the growth performance, digestive functions and immunity of broiler chickens. Anim. Nutr. 4:388-393.

How to Cite
Pratama, A., Mareta, I., Yudiarti, T., Wahyuni, H. I., Widiastuti, E., & Sugiharto, S. (2021). Administration of Fermented Averrhoa bilimbi L. Fruit Filtrate on Growth, Hematological, Intestinal, and Carcass Indices of Broilers. Tropical Animal Science Journal, 44(1), 79-89.