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Growth Performance, Antioxidants, Intestinal Microbial Composition and Histological Effect of Grass Carp (Ctenopharyngodon idella) through diets Enriched to Pomegranate Peel (Punica granatum) Extracts
Corresponding Author(s) : Raad M. Sayed-Lafi
Jurnal Ilmiah Perikanan dan Kelautan, Vol. 16 No. 2 (2024): JURNAL ILMIAH PERIKANAN DAN KELAUTAN
Abstract
Graphical Abstract
Highlight Research
- PPE supported the growth indices like final weight, weight gain, SGR, and FCR.
- PPE affected the total aerobic bacteria or total lactic acid bacteria (LAB) count, but the enteric gram-negative bacteria count was significantly reduced in the experimental groups.
- Add PPE caused a reduced total fungi count in all treated fish.
- The histological examination showed enlargement of the villi, depth of the villi, and an increase in goblet cells for the treatments supplemented with PPE.
Abstract
Pomegranate is considered one of the medicinal herbs rich in antioxidants that can be used in aquaculture to support immunity and health. The objective of this investigation was to ascertain the impact of pomegranate peel (Punica granatum) extract (PPE) on growth performance, the intestinal bacteria count, the total number of fungi and the histological analysis of the grass carp. 105 fingerlings (11.04±0.22g) were distributed among 21 aquariums (60-L) in a completely randomised design (triplicated) and fed diets containing 0, 0.5, and 1% PPE for 70 days at a feeding rate of 3% body weight. A spectrophotometry assessment indicated for PPE that the total phenol content was 151.09 and 175.95 GAE/100 g, and the flavonoid content was 36.04 and 42.89 RE/100 g, respectively. The results of the present work revealed that growth indicators (final weight, weight gain, specific growth rate (SGR), and feed conversion ratio (FCR)) increased (P<0.05) in the PPE group in comparison to the control group. PPE had an impact on the total count of aerobic bacteria or lactic acid bacteria (LAB), but the experimental treatments dramatically decreased the amount of enteric gram-negative bacteria (P<0.05). The total fungi count showed a significant increase in all treated fish (P<0.05). Also, histological examination showed improvement and elongation of the villi, and an increase in goblet cells for the treatments supplemented with PPE. Therefore, it is recommended to use PPE (0.5%) as a diet additive for grass carp to improve their growth performance and health.
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- Aanyu, M., Ondhoro, C. C., Ganda, E., Kato D. G. & Basiita, R. K. (2014). Intestine histology, nutrient digestibility and body composition of Nile tilapia (Oreochromis niloticus) fed on diets with both cotton and sunflower seed cakes. African Journal of Biotechnology, 13(37):3831-3839.
- Abdel Moneim, A. E. (2012). Evaluating the potential role of pomegranate peel in aluminum-induced oxidative stress and histopathological alterations in brain of female rats. Biological Trace Element Research, 150(1):328-336.
- Abdollahzadeh, E. (2011). Poring over the findings, interpersonal authorial engagement in applied linguistics papers. Journal of Pragmatics, 43(1):288-297.
- Abdullah, T., Wahjuningrum, D., & Widanarni, W. (2024). Effect of dietary Canarium indicum L. on the growth, health, and resistance of Asian seabass challenged with Vibrio alginolyticus. Jurnal Ilmiah Perikanan dan Kelautan, 16(1):31-46.
- Akhtar, S., Ismail T., Fraternale, D. & Sestilib, P. (2015). Pomegranate peel and peel extracts, chemistry and food features. Food Chemistry, 174(9):417-425.
- Al-Jandal (2021). The nutritional importance, and biological efficiency of pomegranate peels Punica granatum and its effect on some biochemical blood features of experimental diabetic rats. Ph. D. Thesis. Tikrit, Iraq: Tikrit University (in Ararbic).
- APHA (1998). Standard methods for the examination of water and wastewater. 20th Edition, American public health association, American water works association and water environmental federation, Washington DC.
- Aqil, F., Ahmad, I., & Mehmood, Z. (2006). Antioxidant and free radical scavenging properties of twelve traditionally used Indian medicinal plants. Turkish Journal of Biology, 30(3):177-183.
- Avazeh, A., Adel, M., Shekarabi, S. P. H., Emamadi, H., Dawood, M. A., Omidi, A. H., & Bavarsad, M. (2021). Effects of dietary pomegranate peel meal on the growth performance, blood indices, and innate immune response of rainbow trout (Oncorhynchus mykiss). Annals of Animal Science, 21(1): 233-244.
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- Cabello, F. C. (2006). Heavy use of prophylactic antibiotics in aquaculture: A growing problem for human and animal health and for the environment. Environmental Microbiology, 8(7):1137-1144.
- Charalampopoulos, D., Wang, R., Pandiella, S. S., & Webb, C. (2002). Application of cereals and cereal components in functional foods, a review. International Journal of Food Microbiology, 79(1-2):131-141.
- Christaki, E., Giannenas, I., Bonos, E. & Florou-Paneri, P. (2020). Innovative uses of aromatic plants as natural supplements in nutrition. In P. Florou-Paneri, E. Christaki, & I. Giannenas (Eds.), Feed additives. (pp. 19-34) Cambridge, Massachusetts: Academic Press.
- Chun, O. K., Kim, D. O. & Lee, C. Y. (2003). Superoxide radical scavenging activity of the major polyphenols in fresh plums. Journal of Agriculture and Food Chemistry, 51(27):8067-8072.
- Da Silva, M. R., Natali, M. R. M., & Hahn, N. S. (2012). Histology of the digestive tract of Satanoperca pappaterra (Osteichthyes, Cichlidae). Acta Scientiarum. Biological Sciences, 34(3):319-326.
- De Marco, G., Cappello, T., & Maisano, M. (2023). Histomorphological changes in fish gut in response to prebiotics and probiotics treatment to improve their health status: A review. Animals, 13(18):1-39.
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- Fauzi, A. R., Yuhana, M., Setiawati, M., & Afiff, U. (2024). Effect of dayak onion (Eleutherine bulbosa (Mill.) Urb.) on the immune response
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- Gupta, S. K., Gupta, A., Sarkar, B., Gupta, R., Kumar, M., Kumari, A., & Foysal, M. J. (2023). Pomegranate (Punica granatum) peel extract supplementation in diet influences growth performance, haemato-immunological responses and cytokine expression in pathogen-aggravated Labeo rohita fingerlings. Aquaculture, 562(1):1-10.
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- Mohammadian, T., Mashjoor, S., Lotfi, S., Bakhshi, H., & Ghanei-Motlagh, R. (2022). Mutual effect of culture density and diet administration of pomegranate peel (Punica granatum L.) extracts on biochemical and antioxidant parameters of common carp (Cyprinus carpio) blood serum. Fisheries Science and Technology, 11(3):240-254.
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- Motlagh, A. H., Hajimoradlo, A., Gorbani, R., Agh, N., Safari, O., & Lashkarizadeh-Bami, M. (2017). Reproductive performance and intestinal bacterial changes of Carassius auratus (L. 1758) fed supplemented lactoferrin and Lactobacillus rhamnosus PTCC 1637 diet. Iranian Journal of Ichthyology, 4(2):150-161.
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- Naveena, B. M., Sen, A. R., Vaithiyanathan, S., Babji, Y., & Kondaiah, N. (2008). Comparative efficacy of pomegranate juice, pomegranate rind powder extract and BHT as antioxidants in cooked chicken patties. Meat Science, 80(4):1304-1308.
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References
Aanyu, M., Ondhoro, C. C., Ganda, E., Kato D. G. & Basiita, R. K. (2014). Intestine histology, nutrient digestibility and body composition of Nile tilapia (Oreochromis niloticus) fed on diets with both cotton and sunflower seed cakes. African Journal of Biotechnology, 13(37):3831-3839.
Abdel Moneim, A. E. (2012). Evaluating the potential role of pomegranate peel in aluminum-induced oxidative stress and histopathological alterations in brain of female rats. Biological Trace Element Research, 150(1):328-336.
Abdollahzadeh, E. (2011). Poring over the findings, interpersonal authorial engagement in applied linguistics papers. Journal of Pragmatics, 43(1):288-297.
Abdullah, T., Wahjuningrum, D., & Widanarni, W. (2024). Effect of dietary Canarium indicum L. on the growth, health, and resistance of Asian seabass challenged with Vibrio alginolyticus. Jurnal Ilmiah Perikanan dan Kelautan, 16(1):31-46.
Akhtar, S., Ismail T., Fraternale, D. & Sestilib, P. (2015). Pomegranate peel and peel extracts, chemistry and food features. Food Chemistry, 174(9):417-425.
Al-Jandal (2021). The nutritional importance, and biological efficiency of pomegranate peels Punica granatum and its effect on some biochemical blood features of experimental diabetic rats. Ph. D. Thesis. Tikrit, Iraq: Tikrit University (in Ararbic).
APHA (1998). Standard methods for the examination of water and wastewater. 20th Edition, American public health association, American water works association and water environmental federation, Washington DC.
Aqil, F., Ahmad, I., & Mehmood, Z. (2006). Antioxidant and free radical scavenging properties of twelve traditionally used Indian medicinal plants. Turkish Journal of Biology, 30(3):177-183.
Avazeh, A., Adel, M., Shekarabi, S. P. H., Emamadi, H., Dawood, M. A., Omidi, A. H., & Bavarsad, M. (2021). Effects of dietary pomegranate peel meal on the growth performance, blood indices, and innate immune response of rainbow trout (Oncorhynchus mykiss). Annals of Animal Science, 21(1): 233-244.
Ayyat, M. S., Ayyat, A. M., Naiel, M. A., & Al-Sagheer, A. A. (2020). Reversal effects of some safe dietary supplements on lead contaminated diet induced impaired growth and associated parameters in Nile tilapia. Aquaculture, 515(2):1-8.
Badawi, M. E., & Gomaa, A. M. (2016). Influence of diets supplemented with pomegranate peel extract on performance in Oreochromus niloticus. Japanese Journal of Veterinary Research, 64(Supplement 2):S87-S94.
Cabello, F. C. (2006). Heavy use of prophylactic antibiotics in aquaculture: A growing problem for human and animal health and for the environment. Environmental Microbiology, 8(7):1137-1144.
Charalampopoulos, D., Wang, R., Pandiella, S. S., & Webb, C. (2002). Application of cereals and cereal components in functional foods, a review. International Journal of Food Microbiology, 79(1-2):131-141.
Christaki, E., Giannenas, I., Bonos, E. & Florou-Paneri, P. (2020). Innovative uses of aromatic plants as natural supplements in nutrition. In P. Florou-Paneri, E. Christaki, & I. Giannenas (Eds.), Feed additives. (pp. 19-34) Cambridge, Massachusetts: Academic Press.
Chun, O. K., Kim, D. O. & Lee, C. Y. (2003). Superoxide radical scavenging activity of the major polyphenols in fresh plums. Journal of Agriculture and Food Chemistry, 51(27):8067-8072.
Da Silva, M. R., Natali, M. R. M., & Hahn, N. S. (2012). Histology of the digestive tract of Satanoperca pappaterra (Osteichthyes, Cichlidae). Acta Scientiarum. Biological Sciences, 34(3):319-326.
De Marco, G., Cappello, T., & Maisano, M. (2023). Histomorphological changes in fish gut in response to prebiotics and probiotics treatment to improve their health status: A review. Animals, 13(18):1-39.
El-Sayed, B. M., Hakim, Y., El-Sayed, H. M., & Ali, H. A. (2014). Effect of partial replacement of yellow corn by pomegranate peel with or without allzyme SSF on growth performance and health status of Oreochromis niloticus. World Journal of Fish & Marine Sciences, 6(12):182-189.
Encarnaço, P. (2013). Phytogenics help improve performance in aquatic species.
FAO (2016). FAO-yearbook of fishery statistics: aquaculture production. Rome, Italy: Food and Agriculture Organization of the United Nations.
Fauzi, A. R., Yuhana, M., Setiawati, M., & Afiff, U. (2024). Effect of dayak onion (Eleutherine bulbosa (Mill.) Urb.) on the immune response
and gene expression of Nile tilapia (Oreochromis niloticus) infected with Aeromonas hydrophila. Jurnal Ilmiah Perikanan dan Kelautan, 16(1):1-14.
Gupta, S. K., Gupta, A., Sarkar, B., Gupta, R., Kumar, M., Kumari, A., & Foysal, M. J. (2023). Pomegranate (Punica granatum) peel extract supplementation in diet influences growth performance, haemato-immunological responses and cytokine expression in pathogen-aggravated Labeo rohita fingerlings. Aquaculture, 562(1):1-10.
Hamouda, A. H., & Moustafa, E. M. (2020). Insight on prevailing bacterial diseases affecting grass carp (Ctenopharyngodon idella) at Aswan fish hatchery, Egypt. Alexandria Journal of Veterinary Sciences, 64(1):5-16.
Handa, S. S., Khanuja, S. P. S., Longo, G. & Rakesh, D. D. (2008). Extraction technologies for medicinal and aromatic plants. Trieste, Italy: International Center for Science and High Technology.
Hofstra, D. E. (2014). Grass carp effectiveness and effects–stage 2: Knowledge review. Prepared for the Department of Conservation. Hamilton, New Zealand: National Institute of Water and Atmospheric Research.
Laudadio, V., Passantino, L., Perillo, A., Lopresti, G., Passantino, A., Khan, R. U., & Tufarelli, V. (2012). Productive performance and histological features of intestinal mucosa of broiler chickens fed different dietary protein levels. Poultry Science, 91(1):265-270.
Liu, B., Jia, R., Han, C., Huang, B., & Lei, J. L. (2016). Effects of stocking density on antioxidant status, metabolism and immune response in juvenile turbot (Scophthalmus maximus). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 190(9):1-8.
Lovkova, M. Y., Buzuk, G. N., Sokolova, S. M., & Kliment'eva, N. I. (2001). Chemical features of medicinal plants. Applied Biochemistry & Microbiology, 37(3):229-237.
Malviya, S., Jha, A., & Hettiarachchy, N. (2014). Antioxidant and antibacterial potential of pomegranate peel extracts. Journal of Food Science & Technology, 51(12):4132-4137.
Mashkor, I. M. A. A., & Muhson, A. A. (2014). Total phenol, total flavonoids and antioxidant activity of pomegranate peel. International Journal ChemTech Research, 6(11):4656-4661.
Mohammadian, T., Mashjoor, S., Lotfi, S., Bakhshi, H., & Ghanei-Motlagh, R. (2022). Mutual effect of culture density and diet administration of pomegranate peel (Punica granatum L.) extracts on biochemical and antioxidant parameters of common carp (Cyprinus carpio) blood serum. Fisheries Science and Technology, 11(3):240-254.
Mohammed, H. H., Ebrahim, M., Youssef, M. I., Saleem, A. S. Y., & Abdelkhalek, A. (2024). Behavior and management of carp fish: A review. Open Veterinary Journal, 14(1):1-11.
Moskaug, J. Ø., Carlsen, H., Myhrstad, M. C., & Blomhoff, R. (2005). Polyphenols and glutathione synthesis regulation. The American Journal of Clinical Nutrition, 81(1):277S-283S.
Motlagh, A. H. R., Farhangi, M., Rafiee, G., & Noori, F. (2012). Modulating gut microbiota and digestive enzyme activities of Artemia urmiana by administration of different levels of Bacillus subtilis and Bacillus licheniformis. Aquaculture International, 20(4):693-705.
Motlagh, A. H. R., Sarkheil, M., Safari, O., & Paolucci, M. (2019). Supplementation of dietary apple cider vinegar as an organic acidifier on the growth performance, digestive enzymes and mucosal immunity of green terror (Andinoacara rivulatus). Aquaculture Research, 51(1):197-205.
Motlagh, A. H., Hajimoradlo, A., Gorbani, R., Agh, N., Safari, O., & Lashkarizadeh-Bami, M. (2017). Reproductive performance and intestinal bacterial changes of Carassius auratus (L. 1758) fed supplemented lactoferrin and Lactobacillus rhamnosus PTCC 1637 diet. Iranian Journal of Ichthyology, 4(2):150-161.
Naveena, B. M., Sen, A. R., Vaithiyanathan, S., Babji, Y., & Kondaiah, N. (2008). Comparative efficacy of pomegranate juice, pomegranate rind powder extract and BHT as antioxidants in cooked chicken patties. Meat Science, 80(4):1304-1308.
Naz, S., Siddiqi, R., Ahmad, S., Rasool, S. A., & Sayeed, S. A. (2007). Antibacterial activity directed isolation of compounds from Punica granatum. Journal of Food Science, 72(9):M341-M345.
Ogunkalu, O. (2019). Effects of feed additives in fish feed for improvement of aquaculture. Eurasian Journal of Food Science and Technology, 3(2):49-57.
Oniszczuk, T., Oniszczuk, A., Gondek, E., Guz, L., Puk, K., Kocira, A., Kusz, A., Kasprzak, K., & Wójtowicz, A. (2019). Active polyphenolic compounds, nutrient contents and antioxidant capacity of extruded fish feed containing purple coneflower (Echinacea purpurea (L.) Moench.). Saudi Journal of Biological Sciences, 26(1):24-30.
Öztürk, F., Gündüz, H. & Sürengil, G. (2018). Effects of alginate based coatings with pomegranate peel extract on the microbial quality of mackerel fillets. Journal of Agricultural Sciences, 24(4):445-452.
Prashanth, D., Asha, M. K., & Amit, A. (2001). Antibacterial activity of Punica granatum. Fitoterapia, 72(2):171-173.
Rahbarian, R., Rajabiian, M., Ramshini, H., & Jafari, S. A. (2022). Investigation of the protective effect of pomegranate peel extract in inhibiting the oxidative damage caused by experimental cadmium poisoning in common carp. Journal of Fisheries, 75(1):99-109.
Reddy, M. K., Gupta, S. K., Jacob, M. R., Khan, S. I., & Ferreira, D. (2007). Antioxidant, antimalarial and antimicrobial activities of tannin-rich fractions, ellagitannins and phenolic acids from Punica granatum L. Planta Medica, 53(05):461-467.
Romeis, B. (1989). Microscopic technology. München: Urban und Schwarzenberg.
Salem, M., & Abdel-Ghany, H. M. (2018). Effects of dietary orange peel on growth performance of Nile tilapia (Oreochromis niloticus) fingerlings. Aquaculture studies, 18(2):127-134.
Schultz, P. W., Shriver, C., Tabanico, J. J., & Khazian, A. M. (2004). Implicit connections with nature. Journal of Environmental Psychology, 24(1):31-42.
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