Nephroprotective Effect of Milkfish, Patin, and Snakehead Fish Oil by Suppressing Inflammation and Oxidative Stress in Diabetic Rats
Keywords:
Fish oil, nephroprotective, inflammation, oxidative stress
Abstract
Diabetic nephropathy (DN) has been linked to a number of long-term problems caused by diabetes mellitus. Inflammatory and oxidative stress pathways contribute to DN development and progression. Many studies have shown the preventive advantages of diets rich in substances like anti-inflammatory and antioxidant elements like omega-3 fatty acids (n-3 FA) in preventing DN. Milkfish (Chanos chanos F.), patin (Pangasius micronema Blkr.), and snakehead fish (Chana striata Bloch) are types of fish oils that are known to contain n-3 FA. This study aims to prove the nephroprotective effect of the three types of fish oil in a rat model of diabetes mellitus. Thirty male rats were used in this study. The animals were randomly divided into six groups (n = 5): the non-diabetic group, the diabetes mellitus group, the diabetic with 150 mg/kg metformin orally group, the diabetic with 1000 mg/kg milkfish oil orally group, the diabetic with 1000 mg/kg patin fish oil orally group, and the diabetic with 1000 mg/kg snakehead fish oil orally group. Diabetes models were induced using 65 mg/kg streptozotocin and 230 mg/kg nicotinamide intraperitoneally. The test was carried out for 8 weeks, followed by the observation of the biochemical profiles of blood, urine, oxidative stress, and the immunohistochemistry of the kidneys. A normally and homogeneously distributed test followed by a one-way analysis of variance (ANOVA) and the LSD post hoc test were used to look at the data. At p≤0.05, the data was considered statistically significant. The results showed that serum creatinine levels did not differ significantly after the administration of milkfish, catfish, and snakehead fish oil for 8 weeks (p≥0.05). Different results were shown where the levels of serum BUN, uric acid, urine urea, and microalbumin urine were significantly different after administration of the three types of fish oil (p≤0.05). The same results were shown in oxidative stress (superoxide dismutase, glutathione, and malondialdehyde) and inflammation (interleukin-6 and tumor necrosis factor-α) profiles (p≤0.05). The conclusion is that milkfish, patin, and snakehead fish oils have moderate nephroprotection by suppressing inflammation and oxidative stress.
References
AlFaris, N. A., Alshammari, G. M., Alsayadi, M. M., AlFaris, M. A., & Yahya, M. A. (2020). Antidiabetic and antihyperlipidemic effect of Duvalia corderoyi in rats with streptozotocin-induced diabetes. Saudi Journal of Biological Sciences, 27(3), 925–934. https://doi.org/10.1016/j.sjbs.2020.01.024
Allan, M., McCafferty, K., Sheaff, M., & Yaqoob, M. M. (2023). Identification and management of diabetic nephropathy. Medicine, 51(4), 262–268. https://doi.org/10.1016/j.mpmed.2023.01.005
Araújo, L. S., Silva, M. V. da, Silva, C. A. da, Monteiro, M. L. R., Pereira, L. H. de M., Rocha, L. P., Corrêa, R. R. M., Reis, M. A., & Machado, J. R. (2016). Cytokines and T Helper Cells in Diabetic Nephropathy Pathogenesis. Journal of Diabetes Mellitus, 06(04), Article 04. https://doi.org/10.4236/jdm.2016.64025
Araújo, L. S., Torquato, B. G. S., da Silva, C. A., dos Reis Monteiro, M. L. G., dos Santos Martins, A. L. M., da Silva, M. V., dos Reis, M. A., & Machado, J. R. (2020). Renal expression of cytokines and chemokines in diabetic nephropathy. BMC Nephrology, 21(1), 308. https://doi.org/10.1186/s12882-020-01960-0
Aryaie, M., Sharifi, H., Saber, A., Salehi, F., Etminan, M., Nazemipour, M., & Mansournia, M. A. (2022). Longitudinal causal effect of modified creatinine index on all-cause mortality in patients with end-stage renal disease: Accounting for time-varying confounders using G-estimation. PLOS ONE, 17(8), e0272212. https://doi.org/10.1371/journal.pone.0272212
Bhatti, J. S., Sehrawat, A., Mishra, J., Sidhu, I. S., Navik, U., Khullar, N., Kumar, S., Bhatti, G. K., & Reddy, P. H. (2022). Oxidative stress in the pathophysiology of type 2 diabetes and related complications: Current therapeutics strategies and future perspectives. Free Radical Biology and Medicine, 184, 114–134. https://doi.org/10.1016/j.freeradbiomed.2022.03.019
Bonilla-Méndez, J. R., Hoyos-Concha, J. L., Bonilla-Méndez, J. R., & Hoyos-Concha, J. L. (2018). Methods of extraction refining and concentration of fish oil as a source of omega-3 fatty acids. Ciencia y Tecnología Agropecuaria, 19(3), 645–668. https://doi.org/10.21930/rcta.vol19_num2_art:684
Brosius, F. C., Alpers, C. E., Bottinger, E. P., Breyer, M. D., Coffman, T. M., Gurley, S. B., Harris, R. C., Kakoki, M., Kretzler, M., Leiter, E. H., Levi, M., McIndoe, R. A., Sharma, K., Smithies, O., Susztak, K., Takahashi, N., & Takahashi, T. (2009). Mouse Models of Diabetic Nephropathy. Journal of the American Society of Nephrology : JASN, 20(12), 2503–2512. https://doi.org/10.1681/ASN.2009070721
Cohen, J. B., Tewksbury, C. M., Torres Landa, S., Williams, N. N., & Dumon, K. R. (2019). National Postoperative Bariatric Surgery Outcomes in Patients with Chronic Kidney Disease and End-Stage Kidney Disease. Obesity Surgery, 29(3), 975–982. https://doi.org/10.1007/s11695-018-3604-2
de Assis, A. M., Rech, A., Longoni, A., da Silva Morrone, M., de Bittencourt Pasquali, M. A., Perry, M. L., Souza, D. O., & Moreira, J. C. (2015). Dietary n-3 polyunsaturated fatty acids revert renal responses induced by a combination of 2 protocols that increase the amounts of advanced glycation end product in rats. Nutrition Research, 35(6), 512–522.
Donadio, J. V. J., Grande, J. P., Bergstralh, E. J., Dart, R. A., Larson, T. S., Spencer, D. C., & Group, T. M. N. C. (1999). The Long-Term Outcome of Patients with IgA Nephropathy Treated with Fish Oil in a Controlled Trial. Journal of the American Society of Nephrology, 10(8), 1772. https://doi.org/10.1681/ASN.V1081772
El-Boshy, M., Alsaegh, A., Qasem, A. H., Sindi, R. A., Abdelghany, A. H., Gadalla, H., Reda, D., Azzeh, F., Idris, S., Ahmad, J., & Refaat, B. (2021). Enhanced renoprotective actions of Paricalcitol and omega-3 fatty acids co-therapy against diabetic nephropathy in rat. Journal of Advanced Research. https://doi.org/10.1016/j.jare.2021.08.010
Fathy, S. A., Mohamed, M. R., Ali, M. A. M., EL-Helaly, A. E., & Alattar, A. T. (2019). Influence of IL-6, IL-10, IFN-γ and TNF-α genetic variants on susceptibility to diabetic kidney disease in type 2 diabetes mellitus patients. Biomarkers, 24(1), 43–55. https://doi.org/10.1080/1354750X.2018.1501761
Ghasemi Fard, S., Wang, F., Sinclair, A. J., Elliott, G., & Turchini, G. M. (2019). How does high DHA fish oil affect health? A systematic review of evidence. Critical Reviews in Food Science and Nutrition, 59(11), 1684–1727. https://doi.org/10.1080/10408398.2018.1425978
Gong, Y., Guo, X., & Zhu, Q. (2022). Nephroprotective properties of chitosan/sodium lignosulfonate/Au nanoparticles in streptozotocin-induced nephropathy in mice: Introducing a novel therapeutic drug for the treatment of nephropathy. Arabian Journal of Chemistry, 15(6), 103761. https://doi.org/10.1016/j.arabjc.2022.103761
Guo, Y., Hu, M., Ma, J., Chinnathambi, A., Alharbi, S. A., Shair, O. H. M., & Ge, P. (2021). Protective effect of panaxydol against repeated administration of aristolochic acid on renal function and lipid peroxidation products via activating Keap1-Nrf2/ARE pathway in rat kidney. Journal of Biochemical and Molecular Toxicology, 35(1), e22619. https://doi.org/10.1002/jbt.22619
Haligur, M., Topsakal, S., & Ozmen, O. (2012). Early Degenerative Effects of Diabetes Mellitus on Pancreas, Liver, and Kidney in Rats: An Immunohistochemical Study. Journal of Diabetes Research, 2012, e120645. https://doi.org/10.1155/2012/120645
Han, E., Yun, Y., Kim, G., Lee, Y., Wang, H. J., Lee, B.-W., Cha, B. S., Kim, B. S., & Kang, E. S. (2016). Effects of Omega-3 Fatty Acid Supplementation on Diabetic Nephropathy Progression in Patients with Diabetes and Hypertriglyceridemia. PLOS ONE, 11(5), e0154683. https://doi.org/10.1371/journal.pone.0154683
Hidayah, N., Rohman, A., Mustafidah, M., & Irnawati. (2022). Physicochemical characterization and fatty acid profiles of fish oil from milkfish (Chanos chanos F.). Food Research, 6(2), 265–270. Scopus. https://doi.org/10.26656/fr.2017.6(2).222
Iseki, K., Ikemiya, Y., & Fukiyama, K. (1997). Risk factors of end-stage renal disease and serum creatinine in a community-based mass screening. Kidney International, 51(3), 850–854. https://doi.org/10.1038/ki.1997.119
Itsiopoulos, C., Marx, W., Mayr, H. L., Tatucu-Babet, O. A., Dash, S. R., George, E. S., Trakman, G. L., Kelly, J. T., Thomas, C. J., & Brazionis, L. (2018). The role of omega-3 polyunsaturated fatty acid supplementation in the management of type 2 diabetes mellitus: A narrative review. Journal of Nutrition & Intermediary Metabolism, 14, 42–51. https://doi.org/10.1016/j.jnim.2018.02.002
Keapai, W., Apichai, S., Amornlerdpison, D., & Lailerd, N. (2016). Evaluation of fish oil-rich in MUFAs for anti-diabetic and anti-inflammation potential in experimental type 2 diabetic rats. The Korean Journal of Physiology & Pharmacology, 20(6), 581–593. https://doi.org/10.4196/kjpp.2016.20.6.581
Kishore, L., Kaur, N., & Singh, R. (2017). Nephroprotective effect of Paeonia emodi via inhibition of advanced glycation end products and oxidative stress in streptozotocin–nicotinamide induced diabetic nephropathy. Journal of Food and Drug Analysis, 25(3), 576–588. https://doi.org/10.1016/j.jfda.2016.08.009
Liu, J.-D., Liu, W.-B., Zhang, D.-D., Xu, C.-Y., Zhang, C.-Y., Zheng, X.-C., & Chi, C. (2020). Dietary reduced glutathione supplementation can improve growth, antioxidant capacity, and immunity on Chinese mitten crab, Eriocheir sinensis. Fish & Shellfish Immunology, 100, 300–308. https://doi.org/10.1016/j.fsi.2020.02.064
Mozaffarian, D., & Wu, J. H. Y. (2012). (n-3) Fatty Acids and Cardiovascular Health: Are Effects of EPA and DHA Shared or Complementary? The Journal of Nutrition, 142(3), 614S-625S. https://doi.org/10.3945/jn.111.149633
Nadhiro, U., Subekti, S., Tjahjaningsih, W., & Patmawati. (2018). Quality characteristics of Bali sardinella (Sardinella lemuru) oil purified with bentonite as an adsorbent. IOP Conference Series: Earth and Environmental Science, 137, 012012. https://doi.org/10.1088/1755-1315/137/1/012012
Nugent, J., Aklilu, A., Yamamoto, Y., Simonov, M., Li, F., Biswas, A., Ghazi, L., Greenberg, J. H., Mansour, S. G., Moledina, D. G., & Wilson, F. P. (2021). Assessment of Acute Kidney Injury and Longitudinal Kidney Function After Hospital Discharge Among Patients With and Without COVID-19. JAMA Network Open, 4(3), e211095. https://doi.org/10.1001/jamanetworkopen.2021.1095
Persson, F., & Rossing, P. (2018). Diagnosis of diabetic kidney disease: State of the art and future perspective. Kidney International Supplements, 8(1), 2–7. https://doi.org/10.1016/j.kisu.2017.10.003
Putri, A. R., Rohman, A., & Riyanto, S. (2019). Comparative study of fatty acid profiles in patin (Pangasius micronemus) and gabus (Channa striata) fish oil and its authentication using FTIR spectroscopy combined with chemometrics. International Journal of Applied Pharmaceutics, 55–60. https://doi.org/10.22159/ijap.2019v11i6.34921
Rahmani, A., Maleki, V., Niknafs, B., Tavakoli-Rouzbehani, O. M., & Tarighat-Esfanjani, A. (2022). Effect of Nigella sativa supplementation on kidney function, glycemic control, oxidative stress, inflammation, quality of life, and depression in diabetic hemodialysis patients: Study protocol for a double-blind, randomized controlled trial. Trials, 23(1), 111. https://doi.org/10.1186/s13063-021-05917-y
Sagoo, M. K., & Gnudi, L. (2018). Diabetic nephropathy: Is there a role for oxidative stress? Free Radical Biology and Medicine, 116, 50–63. https://doi.org/10.1016/j.freeradbiomed.2017.12.040
Samsu, N. (2021). Diabetic Nephropathy: Challenges in Pathogenesis, Diagnosis, and Treatment. BioMed Research International, 2021, e1497449. https://doi.org/10.1155/2021/1497449
Sasongko, H., Efendi, N. R., Budihardjo, A., Farida, Y., Amartiwi, T., Rahmawati, A. A., Wicaksono, A., & Sugiyarto. (2017). Solvent and extraction methods effects on the quality of eel ( Anguilla bicolor ) oil. Journal of Physics: Conference Series, 795(1), 012021. https://doi.org/10.1088/1742-6596/795/1/012021
Sasongko, H., Efendi, N. R., & Sugiyarto. (2018). The ethanolic extract of mountain papaya (Vasconcellea pubescens A.DC.) fruit against lipid peroxidation of rat liver tissues. AIP Conference Proceedings, 2019(1), 050001. https://doi.org/10.1063/1.5061894
Sasongko, H., Nurrochmad, A., Nugroho, A. E., & Rohman, A. (2022). Indonesian freshwater fisheries’ oil for health and nutrition applications: A narrative review. Food Research, 6, 501–511. https://doi.org/10.26656/fr.2017.6(2).362
Sasongko, H., Nurrochmad, A., Rohman, A., & Nugroho, A. E. (2022). Characteristic of Streptozotocin-Nicotinamide-Induced Inflammation in A Rat Model of Diabetes-Associated Renal Injury. Open Access Macedonian Journal of Medical Sciences, 10(T8), 16–22.
Sathibabu Uddandrao, V. V., Brahmanaidu, P., Ravindarnaik, R., Suresh, P., Vadivukkarasi, S., & Saravanan, G. (2019). Restorative potentiality of S-allylcysteine against diabetic nephropathy through attenuation of oxidative stress and inflammation in streptozotocin–nicotinamide-induced diabetic rats. European Journal of Nutrition, 58(6), 2425–2437. https://doi.org/10.1007/s00394-018-1795-x
Sayed, A. A. R. (2012). Ferulsinaic Acid Modulates SOD, GSH, and Antioxidant Enzymes in Diabetic Kidney. Evidence-Based Complementary and Alternative Medicine, 2012, e580104. https://doi.org/10.1155/2012/580104
Shapiro, H., Theilla, M., Attal-Singer, J., & Singer, P. (2011). Effects of polyunsaturated fatty acid consumption in diabetic nephropathy. Nature Reviews Nephrology, 7(2), Article 2. https://doi.org/10.1038/nrneph.2010.156
Singh, B., Kumar, A., Singh, H., Kaur, S., Kaur, S., Singh Buttar, H., Arora, S., & Singh, B. (2020). Zingerone produces antidiabetic effects and attenuates diabetic nephropathy by reducing oxidative stress and overexpression of NF-κB, TNF-α, and COX-2 proteins in rats. Journal of Functional Foods, 74, 104199. https://doi.org/10.1016/j.jff.2020.104199
Sugata, M., Wiriadi, P. F., Lucy, J., & Jan, T. T. (2019). Total lipid and omega-3 content in Pangasius catfish (Pangasius pangasius) and milkfish (Chanos chanos) from Indonesia. Malaysian Journal of Nutrition, 25(1), 163–170. Scopus. https://doi.org/10.31246/mjn-2018-0137
Szeto, H. H. (2006). Mitochondria-targeted peptide antioxidants: Novel neuroprotective agents. The AAPS Journal, 8(3), 62. https://doi.org/10.1208/aapsj080362
Tsai, H.-J., Kuo, F.-C., Wu, C.-F., Sun, C.-W., Hsieh, C.-J., Wang, S.-L., Chen, M.-L., Hsieh, H.-M., Chuang, Y.-S., & Wu, M.-T. (2021). Association between two common environmental toxicants (phthalates and melamine) and urinary markers of renal injury in the third trimester of pregnant women: The Taiwan Maternal and Infant Cohort Study (TMICS). Chemosphere, 272, 129925. https://doi.org/10.1016/j.chemosphere.2021.129925
Usta, M., Ersoy, A., Ersoy, C., Ayar, Y., Goksel, G., & Karagoz, I. S. (2020). Effect of omega-3 polyunsaturated fatty acid supplementation on glycemic control and renal function in type 2 diabetic patients with chronic kidney disease. Acta Medica Mediterranea, 36(2), 821–828.
Vitlov Uljević, M., Starčević, K., Mašek, T., Bočina, I., Restović, I., Kević, N., Racetin, A., Kretzschmar, G., Grobe, M., Vukojević, K., Saraga-Babić, M., & Filipović, N. (2019). Dietary DHA/EPA supplementation ameliorates diabetic nephropathy by protecting from distal tubular cell damage. Cell and Tissue Research, 378(2), 301–317. https://doi.org/10.1007/s00441-019-03058-y
Yoo, D., Jung, E., Noh, J., Hyun, H., Seon, S., Hong, S., Kim, D., & Lee, D. (2019). Glutathione-Depleting Pro-Oxidant as a Selective Anticancer Therapeutic Agent. ACS Omega, 4(6), 10070–10077. https://doi.org/10.1021/acsomega.9b00140
Allan, M., McCafferty, K., Sheaff, M., & Yaqoob, M. M. (2023). Identification and management of diabetic nephropathy. Medicine, 51(4), 262–268. https://doi.org/10.1016/j.mpmed.2023.01.005
Araújo, L. S., Silva, M. V. da, Silva, C. A. da, Monteiro, M. L. R., Pereira, L. H. de M., Rocha, L. P., Corrêa, R. R. M., Reis, M. A., & Machado, J. R. (2016). Cytokines and T Helper Cells in Diabetic Nephropathy Pathogenesis. Journal of Diabetes Mellitus, 06(04), Article 04. https://doi.org/10.4236/jdm.2016.64025
Araújo, L. S., Torquato, B. G. S., da Silva, C. A., dos Reis Monteiro, M. L. G., dos Santos Martins, A. L. M., da Silva, M. V., dos Reis, M. A., & Machado, J. R. (2020). Renal expression of cytokines and chemokines in diabetic nephropathy. BMC Nephrology, 21(1), 308. https://doi.org/10.1186/s12882-020-01960-0
Aryaie, M., Sharifi, H., Saber, A., Salehi, F., Etminan, M., Nazemipour, M., & Mansournia, M. A. (2022). Longitudinal causal effect of modified creatinine index on all-cause mortality in patients with end-stage renal disease: Accounting for time-varying confounders using G-estimation. PLOS ONE, 17(8), e0272212. https://doi.org/10.1371/journal.pone.0272212
Bhatti, J. S., Sehrawat, A., Mishra, J., Sidhu, I. S., Navik, U., Khullar, N., Kumar, S., Bhatti, G. K., & Reddy, P. H. (2022). Oxidative stress in the pathophysiology of type 2 diabetes and related complications: Current therapeutics strategies and future perspectives. Free Radical Biology and Medicine, 184, 114–134. https://doi.org/10.1016/j.freeradbiomed.2022.03.019
Bonilla-Méndez, J. R., Hoyos-Concha, J. L., Bonilla-Méndez, J. R., & Hoyos-Concha, J. L. (2018). Methods of extraction refining and concentration of fish oil as a source of omega-3 fatty acids. Ciencia y Tecnología Agropecuaria, 19(3), 645–668. https://doi.org/10.21930/rcta.vol19_num2_art:684
Brosius, F. C., Alpers, C. E., Bottinger, E. P., Breyer, M. D., Coffman, T. M., Gurley, S. B., Harris, R. C., Kakoki, M., Kretzler, M., Leiter, E. H., Levi, M., McIndoe, R. A., Sharma, K., Smithies, O., Susztak, K., Takahashi, N., & Takahashi, T. (2009). Mouse Models of Diabetic Nephropathy. Journal of the American Society of Nephrology : JASN, 20(12), 2503–2512. https://doi.org/10.1681/ASN.2009070721
Cohen, J. B., Tewksbury, C. M., Torres Landa, S., Williams, N. N., & Dumon, K. R. (2019). National Postoperative Bariatric Surgery Outcomes in Patients with Chronic Kidney Disease and End-Stage Kidney Disease. Obesity Surgery, 29(3), 975–982. https://doi.org/10.1007/s11695-018-3604-2
de Assis, A. M., Rech, A., Longoni, A., da Silva Morrone, M., de Bittencourt Pasquali, M. A., Perry, M. L., Souza, D. O., & Moreira, J. C. (2015). Dietary n-3 polyunsaturated fatty acids revert renal responses induced by a combination of 2 protocols that increase the amounts of advanced glycation end product in rats. Nutrition Research, 35(6), 512–522.
Donadio, J. V. J., Grande, J. P., Bergstralh, E. J., Dart, R. A., Larson, T. S., Spencer, D. C., & Group, T. M. N. C. (1999). The Long-Term Outcome of Patients with IgA Nephropathy Treated with Fish Oil in a Controlled Trial. Journal of the American Society of Nephrology, 10(8), 1772. https://doi.org/10.1681/ASN.V1081772
El-Boshy, M., Alsaegh, A., Qasem, A. H., Sindi, R. A., Abdelghany, A. H., Gadalla, H., Reda, D., Azzeh, F., Idris, S., Ahmad, J., & Refaat, B. (2021). Enhanced renoprotective actions of Paricalcitol and omega-3 fatty acids co-therapy against diabetic nephropathy in rat. Journal of Advanced Research. https://doi.org/10.1016/j.jare.2021.08.010
Fathy, S. A., Mohamed, M. R., Ali, M. A. M., EL-Helaly, A. E., & Alattar, A. T. (2019). Influence of IL-6, IL-10, IFN-γ and TNF-α genetic variants on susceptibility to diabetic kidney disease in type 2 diabetes mellitus patients. Biomarkers, 24(1), 43–55. https://doi.org/10.1080/1354750X.2018.1501761
Ghasemi Fard, S., Wang, F., Sinclair, A. J., Elliott, G., & Turchini, G. M. (2019). How does high DHA fish oil affect health? A systematic review of evidence. Critical Reviews in Food Science and Nutrition, 59(11), 1684–1727. https://doi.org/10.1080/10408398.2018.1425978
Gong, Y., Guo, X., & Zhu, Q. (2022). Nephroprotective properties of chitosan/sodium lignosulfonate/Au nanoparticles in streptozotocin-induced nephropathy in mice: Introducing a novel therapeutic drug for the treatment of nephropathy. Arabian Journal of Chemistry, 15(6), 103761. https://doi.org/10.1016/j.arabjc.2022.103761
Guo, Y., Hu, M., Ma, J., Chinnathambi, A., Alharbi, S. A., Shair, O. H. M., & Ge, P. (2021). Protective effect of panaxydol against repeated administration of aristolochic acid on renal function and lipid peroxidation products via activating Keap1-Nrf2/ARE pathway in rat kidney. Journal of Biochemical and Molecular Toxicology, 35(1), e22619. https://doi.org/10.1002/jbt.22619
Haligur, M., Topsakal, S., & Ozmen, O. (2012). Early Degenerative Effects of Diabetes Mellitus on Pancreas, Liver, and Kidney in Rats: An Immunohistochemical Study. Journal of Diabetes Research, 2012, e120645. https://doi.org/10.1155/2012/120645
Han, E., Yun, Y., Kim, G., Lee, Y., Wang, H. J., Lee, B.-W., Cha, B. S., Kim, B. S., & Kang, E. S. (2016). Effects of Omega-3 Fatty Acid Supplementation on Diabetic Nephropathy Progression in Patients with Diabetes and Hypertriglyceridemia. PLOS ONE, 11(5), e0154683. https://doi.org/10.1371/journal.pone.0154683
Hidayah, N., Rohman, A., Mustafidah, M., & Irnawati. (2022). Physicochemical characterization and fatty acid profiles of fish oil from milkfish (Chanos chanos F.). Food Research, 6(2), 265–270. Scopus. https://doi.org/10.26656/fr.2017.6(2).222
Iseki, K., Ikemiya, Y., & Fukiyama, K. (1997). Risk factors of end-stage renal disease and serum creatinine in a community-based mass screening. Kidney International, 51(3), 850–854. https://doi.org/10.1038/ki.1997.119
Itsiopoulos, C., Marx, W., Mayr, H. L., Tatucu-Babet, O. A., Dash, S. R., George, E. S., Trakman, G. L., Kelly, J. T., Thomas, C. J., & Brazionis, L. (2018). The role of omega-3 polyunsaturated fatty acid supplementation in the management of type 2 diabetes mellitus: A narrative review. Journal of Nutrition & Intermediary Metabolism, 14, 42–51. https://doi.org/10.1016/j.jnim.2018.02.002
Keapai, W., Apichai, S., Amornlerdpison, D., & Lailerd, N. (2016). Evaluation of fish oil-rich in MUFAs for anti-diabetic and anti-inflammation potential in experimental type 2 diabetic rats. The Korean Journal of Physiology & Pharmacology, 20(6), 581–593. https://doi.org/10.4196/kjpp.2016.20.6.581
Kishore, L., Kaur, N., & Singh, R. (2017). Nephroprotective effect of Paeonia emodi via inhibition of advanced glycation end products and oxidative stress in streptozotocin–nicotinamide induced diabetic nephropathy. Journal of Food and Drug Analysis, 25(3), 576–588. https://doi.org/10.1016/j.jfda.2016.08.009
Liu, J.-D., Liu, W.-B., Zhang, D.-D., Xu, C.-Y., Zhang, C.-Y., Zheng, X.-C., & Chi, C. (2020). Dietary reduced glutathione supplementation can improve growth, antioxidant capacity, and immunity on Chinese mitten crab, Eriocheir sinensis. Fish & Shellfish Immunology, 100, 300–308. https://doi.org/10.1016/j.fsi.2020.02.064
Mozaffarian, D., & Wu, J. H. Y. (2012). (n-3) Fatty Acids and Cardiovascular Health: Are Effects of EPA and DHA Shared or Complementary? The Journal of Nutrition, 142(3), 614S-625S. https://doi.org/10.3945/jn.111.149633
Nadhiro, U., Subekti, S., Tjahjaningsih, W., & Patmawati. (2018). Quality characteristics of Bali sardinella (Sardinella lemuru) oil purified with bentonite as an adsorbent. IOP Conference Series: Earth and Environmental Science, 137, 012012. https://doi.org/10.1088/1755-1315/137/1/012012
Nugent, J., Aklilu, A., Yamamoto, Y., Simonov, M., Li, F., Biswas, A., Ghazi, L., Greenberg, J. H., Mansour, S. G., Moledina, D. G., & Wilson, F. P. (2021). Assessment of Acute Kidney Injury and Longitudinal Kidney Function After Hospital Discharge Among Patients With and Without COVID-19. JAMA Network Open, 4(3), e211095. https://doi.org/10.1001/jamanetworkopen.2021.1095
Persson, F., & Rossing, P. (2018). Diagnosis of diabetic kidney disease: State of the art and future perspective. Kidney International Supplements, 8(1), 2–7. https://doi.org/10.1016/j.kisu.2017.10.003
Putri, A. R., Rohman, A., & Riyanto, S. (2019). Comparative study of fatty acid profiles in patin (Pangasius micronemus) and gabus (Channa striata) fish oil and its authentication using FTIR spectroscopy combined with chemometrics. International Journal of Applied Pharmaceutics, 55–60. https://doi.org/10.22159/ijap.2019v11i6.34921
Rahmani, A., Maleki, V., Niknafs, B., Tavakoli-Rouzbehani, O. M., & Tarighat-Esfanjani, A. (2022). Effect of Nigella sativa supplementation on kidney function, glycemic control, oxidative stress, inflammation, quality of life, and depression in diabetic hemodialysis patients: Study protocol for a double-blind, randomized controlled trial. Trials, 23(1), 111. https://doi.org/10.1186/s13063-021-05917-y
Sagoo, M. K., & Gnudi, L. (2018). Diabetic nephropathy: Is there a role for oxidative stress? Free Radical Biology and Medicine, 116, 50–63. https://doi.org/10.1016/j.freeradbiomed.2017.12.040
Samsu, N. (2021). Diabetic Nephropathy: Challenges in Pathogenesis, Diagnosis, and Treatment. BioMed Research International, 2021, e1497449. https://doi.org/10.1155/2021/1497449
Sasongko, H., Efendi, N. R., Budihardjo, A., Farida, Y., Amartiwi, T., Rahmawati, A. A., Wicaksono, A., & Sugiyarto. (2017). Solvent and extraction methods effects on the quality of eel ( Anguilla bicolor ) oil. Journal of Physics: Conference Series, 795(1), 012021. https://doi.org/10.1088/1742-6596/795/1/012021
Sasongko, H., Efendi, N. R., & Sugiyarto. (2018). The ethanolic extract of mountain papaya (Vasconcellea pubescens A.DC.) fruit against lipid peroxidation of rat liver tissues. AIP Conference Proceedings, 2019(1), 050001. https://doi.org/10.1063/1.5061894
Sasongko, H., Nurrochmad, A., Nugroho, A. E., & Rohman, A. (2022). Indonesian freshwater fisheries’ oil for health and nutrition applications: A narrative review. Food Research, 6, 501–511. https://doi.org/10.26656/fr.2017.6(2).362
Sasongko, H., Nurrochmad, A., Rohman, A., & Nugroho, A. E. (2022). Characteristic of Streptozotocin-Nicotinamide-Induced Inflammation in A Rat Model of Diabetes-Associated Renal Injury. Open Access Macedonian Journal of Medical Sciences, 10(T8), 16–22.
Sathibabu Uddandrao, V. V., Brahmanaidu, P., Ravindarnaik, R., Suresh, P., Vadivukkarasi, S., & Saravanan, G. (2019). Restorative potentiality of S-allylcysteine against diabetic nephropathy through attenuation of oxidative stress and inflammation in streptozotocin–nicotinamide-induced diabetic rats. European Journal of Nutrition, 58(6), 2425–2437. https://doi.org/10.1007/s00394-018-1795-x
Sayed, A. A. R. (2012). Ferulsinaic Acid Modulates SOD, GSH, and Antioxidant Enzymes in Diabetic Kidney. Evidence-Based Complementary and Alternative Medicine, 2012, e580104. https://doi.org/10.1155/2012/580104
Shapiro, H., Theilla, M., Attal-Singer, J., & Singer, P. (2011). Effects of polyunsaturated fatty acid consumption in diabetic nephropathy. Nature Reviews Nephrology, 7(2), Article 2. https://doi.org/10.1038/nrneph.2010.156
Singh, B., Kumar, A., Singh, H., Kaur, S., Kaur, S., Singh Buttar, H., Arora, S., & Singh, B. (2020). Zingerone produces antidiabetic effects and attenuates diabetic nephropathy by reducing oxidative stress and overexpression of NF-κB, TNF-α, and COX-2 proteins in rats. Journal of Functional Foods, 74, 104199. https://doi.org/10.1016/j.jff.2020.104199
Sugata, M., Wiriadi, P. F., Lucy, J., & Jan, T. T. (2019). Total lipid and omega-3 content in Pangasius catfish (Pangasius pangasius) and milkfish (Chanos chanos) from Indonesia. Malaysian Journal of Nutrition, 25(1), 163–170. Scopus. https://doi.org/10.31246/mjn-2018-0137
Szeto, H. H. (2006). Mitochondria-targeted peptide antioxidants: Novel neuroprotective agents. The AAPS Journal, 8(3), 62. https://doi.org/10.1208/aapsj080362
Tsai, H.-J., Kuo, F.-C., Wu, C.-F., Sun, C.-W., Hsieh, C.-J., Wang, S.-L., Chen, M.-L., Hsieh, H.-M., Chuang, Y.-S., & Wu, M.-T. (2021). Association between two common environmental toxicants (phthalates and melamine) and urinary markers of renal injury in the third trimester of pregnant women: The Taiwan Maternal and Infant Cohort Study (TMICS). Chemosphere, 272, 129925. https://doi.org/10.1016/j.chemosphere.2021.129925
Usta, M., Ersoy, A., Ersoy, C., Ayar, Y., Goksel, G., & Karagoz, I. S. (2020). Effect of omega-3 polyunsaturated fatty acid supplementation on glycemic control and renal function in type 2 diabetic patients with chronic kidney disease. Acta Medica Mediterranea, 36(2), 821–828.
Vitlov Uljević, M., Starčević, K., Mašek, T., Bočina, I., Restović, I., Kević, N., Racetin, A., Kretzschmar, G., Grobe, M., Vukojević, K., Saraga-Babić, M., & Filipović, N. (2019). Dietary DHA/EPA supplementation ameliorates diabetic nephropathy by protecting from distal tubular cell damage. Cell and Tissue Research, 378(2), 301–317. https://doi.org/10.1007/s00441-019-03058-y
Yoo, D., Jung, E., Noh, J., Hyun, H., Seon, S., Hong, S., Kim, D., & Lee, D. (2019). Glutathione-Depleting Pro-Oxidant as a Selective Anticancer Therapeutic Agent. ACS Omega, 4(6), 10070–10077. https://doi.org/10.1021/acsomega.9b00140
Published
2024-03-25
How to Cite
Sasongko, H., Endro Nugroho , A., Nurrochmad, A., & Rohman, A. (2024). Nephroprotective Effect of Milkfish, Patin, and Snakehead Fish Oil by Suppressing Inflammation and Oxidative Stress in Diabetic Rats . Indonesian Journal of Pharmacy, 35(1), 63-73. https://doi.org/10.22146/ijp.7725
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Research Article
