Administration of Fermented Averrhoa bilimbi L. Fruit Filtrate on Growth, Hematological, Intestinal, and Carcass Indices of Broilers
Abstract
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.
References
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. http://dx.doi.org/10.4314/sajas.v45i5.6
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. http://dx.doi.org/10.1016/j.atherosclerosis.2015.06.030
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. https://doi.org/10.3382/ps.2008-00244
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. https://doi.org/10.3382/ps.2012-02813
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. https://doi.org/10.3382/ps.2013-03763
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. https://doi.org/10.2478/v10220-012-0061-z
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. https://doi.org/10.3329/sjps.v2i2.5821
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. https://doi.org/10.1590/1806-9061-2016-0375
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. https://doi.org/10.1399/eps.2014.56
Ferdous, F., D. Maurice, & T. Scott. 2008. Broiler chick thrombocyte response to lipopolysaccharide. Poult. Sci. 87:61-63. https://doi.org/10.3382/ps.2007-00356
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. https://doi.org/10.3382/ps/pew164
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:/doi.org/10.1186/s40168-017-0315-1
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. https://doi.org/10.5398/tasj.2018.41.3.200
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
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. http://www.lrrd.org/lrrd30/11/sgh_u30183.html
Khan, S. H, & J. Iqbal. 2016. Recent advances in the role of organic acids in poultry nutrition. J. Appl. Anim. Res. 44:359-369. https://doi.org/10.1080/09712119.2015.1079527
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. https://doi.org/10.3923/ajava.2014.71.76
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. https://doi.org/10.20546/ijcmas.2020.905.255
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. https://doi.org/10.3382/japr/pfw073
Nourmohammadi, R., & H. Khosravinia. 2015. Acidic stress caused by dietary administration of citric acid in broiler chickens. Arch. Anim. Breed. 58:309-315. https://doi.org/10.5194/aab-58-309-2015
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. https://doi.org/10.1016/j.aninu.2015.07.002
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. https://doi.org/10.1016/j.aninu.2018.03.007
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. https://doi.org/10.1111/jpn.13282
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. https://doi.org/10.1038/s41598-019-38725-1
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. https://doi.org/10.1088/1742-6596/1073/3/032012
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. https://doi.org/10.1111/jpn.12858
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. https://doi.org/10.3389/fmicb.2019.01091
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. https://doi.org/10.1016/j.aninu.2018.07.004
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. https://doi.org/10.1071/AN11081
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., 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. https://doi.org/10.1515/aoas-2016-0062
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. https://doi.org/10.5455/javar.2018.e284
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., 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. https://doi.org/10.5398/tasj.2019.42.2.113
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
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. http://www.lrrd.org/lrrd31/9/endwi31134.html
Widyastuti, Y., Rohmatussolihat, & A. Febrisiantosa. 2014. The role of lactic acid bacteria in milk fermentation. Food Nutr. Sci. 5:435-442. https://doi.org/10.4236/fns.2014.54051
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. https://doi.org/10.21776/ub.jiip.2019.029.01.02
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. https://doi.org/10.1002/mbo3.708
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. https://doi.org/10.1093/ps/82.6.1030
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. https://doi.org/10.1016/j.aninu.2018.04.005
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