Analysis of Amino Acid Profiles in Bone, Oil, and Muscle Tissue and Wound Healing Activity of Pangasius hypophthalmus Oil in Rattus norvegicus
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Submitted
10 September 2024
10 September 2024
Published
28 February 2025
28 February 2025
Abstract
Patin (Pangasius hypophthalmus), a commercially important freshwater fish, is a rich source of protein containing both essential and non-essential amino acids, crucial for various biological functions. This study aimed to determine the amino acid composition of muscle tissue, oil, and bones of P. hypophthalmus and evaluate the wound healing potential of its oil extract in Rattus norvegicus. High-Performance Liquid Chromatography was employed to quantify the levels of essential and non-essential amino acids in each tissue. Results revealed that P. hypophthalmus oil exhibited the highest total amino acid content, particularly rich in histidine, arginine, and lysine. The wound healing activity of P. hypophthalmus oil extract was assessed in a rodent model, demonstrating a significant reduction in wound area (0.62-0.84 mm) and an impressive wound healing percentage (79-84.45%). These findings suggest that different parts of P. hypophthalmus possess valuable nutritional and therapeutic properties. Notably, the high amino acid content of P. hypophthalmus oil, particularly essential amino acids, highlights its potential as a promising source for developing pharmaceutical products, including amino acid supplements, wound healing agents, and formulations for metabolic support. Further research is warranted to fully explore the therapeutic potential of P. hypophthalmus oil and its bioactive components.
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References
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11. Arribas-López E, Zand N, Ojo O, Snowden MJ, Kochhar T. The Effect of Amino Acids on Wound Healing: A Systematic Review and Meta-Analysis on Arginine and Glutamine. Nutrients. 2021;13(8):2498. DOI: 10.3390/nu13082498; PMCID: PMC8399682; PMID: 34444657
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15. Liu C, Yan Z, Zhang X, Xia T, Ashaolu JO, Olatunji OJ, et al. Food-derived bioactive peptides potentiating therapeutic intervention in rheumatoid arthritis. Heliyon. 2024;10(10):e31104. DOI: 10.1016/j.heliyon.2024.e31104; PMCID: PMC11109807; PMID: 38778960
16. Rathod NB, Pagarkar AU, Pujari KH, Shingare PE, Satam SB, Phadke GG, et al. Status of Valuable Components from Pangasius: A Review. Int J Curr Microbiol App Sci. 2018;7(4):2106-20. DOI: 10.20546/ijcmas.2018.704.241
17. Silva JR, Burger B, Kühl CMC, Candreva T, Anjos MBPD, Rodrigues HG. Wound Healing and Omega-6 Fatty Acids: From Inflammation to Repair. Mediators Inflamm. 2018;2018:2503950. DOI: 10.1155/2018/2503950; PMCID: PMC5925018; PMID: 29849484
18. Huang TH, Wang PW, Yang SC, Chou WL, Fang JY. Cosmetic and Therapeutic Applications of Fish Oil's Fatty Acids on the Skin. Mar Drugs. 2018;16(8):256. DOI: 10.3390/md16080256; PMCID: PMC6117694; PMID: 30061538
19. Rinawati R, Agustina R, Suhartono E. Penyembuhan luka dengan penurunan eritema pada tikus putih (Rattus norvegicus) yang diberi getah batang jarak cina (Jatropha multifida L). Dunia Keperawatan J Keperawatan Kesehatan. 2015;3(1):1-11.
20. Divadi A, Yuliani SH. Pembuatan dan Uji Aktivitas Sediaan Gel Scarless Wound dengan Ekstrak Binahong dan Zat Aktif Piroxicam. J Pharm Sci Commun. 2016;12(2):41-7. DOI: 10.24071/jpsc.122130
21. Rahmanda A. Uji Efek Penyembuhan Luka Fase Minyak Ekstrak Ikan Toman (Channa micropeltes) pada Tikus Putih Jantan Wistar yang Diberi Luka Sayat. J Mahasiswa Farmasi Fakultas Kedokteran UNTAN. 2014;1(1):1-11.
22. Moro J, Tomé D, Schmidely P, Demersay TC, Azzout-Marniche D. Histidine: A Systematic Review on Metabolism and Physiological Effects in Human and Different Animal Species. Nutrients. 2020;12(5):1414. DOI: 10.3390/nu12051414; PMCID: PMC7284872; PMID: 32423010
23. Petraru A, Amariei S. Rapeseed-An Important Oleaginous Plant in the Oil Industry and the Resulting Meal a Valuable Source of Bioactive Compounds. Plants. 2024;13(21):3085. DOI: 10.3390/plants13213085; PMCID: PMC11548519; PMID: 39520003
24. Nurfaidah, Asikin AN, Kasmiati, Angraeni. Amino acid profile and potential utilization purposes of albumin from four types of freshwater fish in Makassar, South Sulawesi, Indonesia. Biodiversitas. 2024;25(11):4199-207. DOI: 10.13057/biodiv/d251119
25. Torsabo D, Ishak SD, Noordin NM, Waiho K, Koh ICC, Yazed MA, et al. Optimizing reproductive performance in pangasius catfish broodstock: A review of dietary and molecular strategies. Vet Anim Sci. 2024;25:100375. DOI: 10.1016/j.vas.2024.100375; PMCID: PMC11245938; PMID: 39005967
26. Mittendorfer B, Volpi E, Wolfe RR. Whole body and skeletal muscle glutamine metabolism in healthy subjects. Am J Physiol Endocrinol Metab. 2001;280(2):E23-33. DOI: 10.1152/ajpendo.2001.280.2.e323; PMCID: PMC3425386; PMID: 11158937
27. Walker MC, van der Donk WA. The many roles of glutamate in metabolism. J Ind Microbiol Biotechnol. 2016;43(2-3):419-30. DOI: 10.1007/s10295-015-1665-y; PMCID: PMC4753154; PMID: 26323613
28. Boutard V, Fouqueray B, Philippe C, Perez J, Baud L. Fish oil supplementation and essential fatty acid deficiency reduce nitric oxide synthesis by rat macrophages. Kidney Int. 1994;46(5):1280-6. DOI: 10.1038/ki.1994.395; PMID: 7531789
29. Zhao Z, Wang Y, Li Q, Zhao H, Duan Y, Wu X, et al. Effects of the photovoltaic fishery culture model on muscle nutritional quality and volatile flavor compounds of Litopenaeus vannamei. Heliyon. 2024;10(15):e34797. DOI: 10.1016/j.heliyon.2024.e34797; PMCID: PMC11332832; PMID: 39161840
30. Gambardella J, Khonkar W, Morelli MB, Wang X, Santulli G, Trimarco V. Arginine and Endothelial Function. Biomedicines. 2020;8(8):277. DOI: 10.3390/biomedicines8080277; PMCID: PMC7460461; PMID: 32781796
31. Gornik HL, Creager MA. Arginine and endothelial and vascular health. J Nutr. 2004;134(10 Suppl):2880-S-7S. DOI: 10.1093/jn/134.10.2880s; PMID: 15465805
32. Langendörfer LJ, Avdylaj B, Hensel O, Diakité D. Design of Plant-Based Food: Influences of Macronutrients and Amino Acid Composition on the Techno-Functional Properties of Legume Proteins. 2023;12(20):3787. DOI: 10.3390/foods12203787; PMCID: PMC10606351; PMID: 37893680
33. Wu G, Meininger CJ, McNeal CJ, Bazer FW, Rhoads JM. Role of L-Arginine in Nitric Oxide Synthesis and Health in Humans. Adv Exp Med Biol. 2021;1332:167-87. DOI: 10.1007/978-3-030-74180-8_10; PMID: 34251644
34. Barbul A, Lazarou SA, Efron DT, Wasserkrug HL, Efron G. Arginine enhances wound healing and lymphocyte immune responses in humans. Surgery. 1990;108(2):331-6. PMID: 2382229
35. Landén NX, Li D, Ståhle M. Transition from inflammation to proliferation: a critical step during wound healing. Cell Mol Life Sci. 2016;73(20):3861-85. DOI: 10.1007/s00018-016-2268-0; PMCID: PMC5021733; PMID: 27180275
36. Segalla GV, Teixeira ST, Rogero MM. Nutritional therapy and wound healing in pressure injury situations: an integrative review. Nutrire. 2021;46:21. DOI: 10.1186/s41110-021-00147-3
37. Ikhsan AN, Irnawati I, Lestari LA, Erwanto Y, Rohman A. Simultaneous analysis of patin fish oil (Pangasius micronemus) and bandeng (Chanos chanos) fish oil using FTIR spectroscopy and chemometrics. Food Res. 2022;6(3):262-8. DOI: 10.26656/fr.2017.6(3).353
38. Lei XX, Cheng LHH, Lin HY, Yang Y, Lu YY, Pang MR, et al. The minimal active domain of human salivary histatin 1 is efficacious in promoting acute skin wound healing. Mil Med Res. 2022;9(1):41. DOI: 10.1186/s40779-022-00398-9; PMCID: PMC9287874; PMID: 35841072
39. Murakami H, Shimbo K, Inoue Y, Takino Y, Kobayashi H. Importance of amino acid composition to improve skin collagen protein synthesis rates in UV-irradiated mice. Amino Acids. 2012;42(6):2481-9. DOI: 10.1007/s00726-011-1059-z; PMCID: PMC3351609; PMID: 21861170
40. Lim JM, Kim G, Levine RL. Methionine in Proteins: It's Not Just for Protein Initiation Anymore. Neurochem Res. 2019;44(1):247-57. DOI: 10.1007/s11064-017-2460-0; PMCID: PMC6446232; PMID: 29327308
41. Holeček M. Histidine in Health and Disease: Metabolism, Physiological Importance, and Use as a Supplement. Nutrients. 2020;12(3):848. DOI: 10.3390/nu12030848; PMCID: PMC7146355; PMID: 32235743
42. Sudha C, Ahilan B, Felix N, Uma A, Chidambaram P, Prabu E. Replacement of fish oil with black soldier fly larvae oil and vegetable oils: Effects of growth, whole-body fatty acid profile, digestive enzyme activity, haemato-biochemical responses and muscle growth-related gene expression of juvenile striped catfish, Pangasianodon hypophthalmus. Aquac Res. 2022;53(8):3097-111. DOI: 10.1111/are.15823
43. Hwang W, Lei W, Katritsis NM, MacMahon M, Chapman K, Han N. Current and prospective computational approaches and challenges for developing COVID-19 vaccines. Adv Drug Deliv Rev. 2021;172:249-74. DOI: 10.1016/j.addr.2021.02.004; PMCID: PMC7871111; PMID: 33561453
44. Tardy AL, Pouteau E, Marquez D, Yilmaz C, Scholey A. Vitamins and Minerals for Energy, Fatigue and Cognition: A Narrative Review of the Biochemical and Clinical Evidence. Nutrients. 2020;12(1):228. DOI: 10.3390/nu12010228; PMCID: PMC7019700; PMID: 31963141
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2. Atanasov AG, Waltenberger B, Pferschy-Wenzig EM, Linder T, Wawrosch C, Uhrin P, et al. Discovery and resupply of pharmacologically active plant-derived natural products: A review. Biotechnol Adv. 2015;33(8):1582-614. DOI: 10.1016/j.biotechadv.2015.08.001; PMCID: PMC4748402; PMID: 26281720
3. Das P, Dutta A, Panchali T, Khatun A, Kar R, Das TK, et al. Advances in therapeutic applications of fish oil: A review. Meas Food. 2024;13:100142. DOI: 10.1016/j.meafoo.2024.100142
4. Mohanty BP, Mahanty A, Ganguly S, Sankar TV, Chakraborty K, Rangasamy A, et al. Nutritional composition of food fishes and their importance in providing food and nutritional security. Food Chem. 2019;293:561-70. DOI: 10.1016/j.foodchem.2017.11.039; PMID: 31151648
5. Nguyen HT, Bao HND, Dang HTT, Tómasson T, Arason S, Gudjónsdóttir M. Protein Recovery of Tra Catfish (Pangasius hypophthalmus) Protein-Rich Side Streams by the pH-Shift Method. Foods. 2022;11(11):1531. DOI: 10.3390/foods11111531; PMCID: PMC9180071; PMID: 35681281
6. Ashraf SA, Adnan M, Patel M, Siddiqui AJ, Sachidanandan M, Snoussi M, et al. Fish-based Bioactives as Potent Nutraceuticals: Exploring the Therapeutic Perspective of Sustainable Food from the Sea. Mar Drugs. 2020;18(5):265. DOI: 10.3390/md18050265; PMCID: PMC7281228; PMID: 32443645
7. McDaniel JC, Belury M, Ahijevych K, Blakely W. Omega-3 fatty acids effect on wound healing. Wound Repair Regen. 2008;16(3):337-45. DOI: 10.1111/j.1524-475x.2008.00388.x; PMCID: PMC2967211; PMID: 18471252
8. Bano S, Khan N, Fatima M, Khalique A, Arslan M, Nazir S, et al. Enhancing farmed striped catfish (Pangasianodon hypophthalmus) robustness through dietary β-glucan. PLoS One. 2024;19(3):e0298414. DOI: 10.1371/journal.pone.0298414; PMCID: PMC10939287; PMID: 38483918
9. Choudhary V, Choudhary M, Bollag WB. Exploring Skin Wound Healing Models and the Impact of Natural Lipids on the Healing Process. Int J Mol Sci. 2024;25(7):3790. DOI: 10.3390/ijms25073790; PMCID: PMC11011291; PMID: 38612601
10. Eming SA, Murray PJ, Pearce EJ. Metabolic orchestration of the wound healing response. Cell Metab. 2021;33(9):1726-43. DOI: 10.1016/j.cmet.2021.07.017; PMID: 34384520
11. Arribas-López E, Zand N, Ojo O, Snowden MJ, Kochhar T. The Effect of Amino Acids on Wound Healing: A Systematic Review and Meta-Analysis on Arginine and Glutamine. Nutrients. 2021;13(8):2498. DOI: 10.3390/nu13082498; PMCID: PMC8399682; PMID: 34444657
12. Gao J, Cahill CM, Huang X, Roffman JL, Lamon-Fava S, Fava M, et al. S-Adenosyl Methionine and Transmethylation Pathways in Neuropsychiatric Diseases Throughout Life. Neurotherapeutics. 2018;15(1):156-75. DOI: 10.1007/s13311-017-0593-0; PMCID: PMC5794704; PMID: 29340929
13. Srivastava GK, Martinez-Rodriguez S, Fadilah NIM, Hao DLQ, Markey G, Shukla P, et al. Progress in Wound-Healing Products Based on Natural Compounds, Stem Cells, and MicroRNA-Based Biopolymers in the European, USA, and Asian Markets: Opportunities, Barriers, and Regulatory Issues. Polymers. 2024;16(9):1280. DOI: 10.3390/polym16091280; PMCID: PMC11085499; PMID: 38732749
14. Simopoulos AP. Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr. 2002;21(6):495-505. DOI: 10.1080/07315724.2002.10719248; PMID: 12480795
15. Liu C, Yan Z, Zhang X, Xia T, Ashaolu JO, Olatunji OJ, et al. Food-derived bioactive peptides potentiating therapeutic intervention in rheumatoid arthritis. Heliyon. 2024;10(10):e31104. DOI: 10.1016/j.heliyon.2024.e31104; PMCID: PMC11109807; PMID: 38778960
16. Rathod NB, Pagarkar AU, Pujari KH, Shingare PE, Satam SB, Phadke GG, et al. Status of Valuable Components from Pangasius: A Review. Int J Curr Microbiol App Sci. 2018;7(4):2106-20. DOI: 10.20546/ijcmas.2018.704.241
17. Silva JR, Burger B, Kühl CMC, Candreva T, Anjos MBPD, Rodrigues HG. Wound Healing and Omega-6 Fatty Acids: From Inflammation to Repair. Mediators Inflamm. 2018;2018:2503950. DOI: 10.1155/2018/2503950; PMCID: PMC5925018; PMID: 29849484
18. Huang TH, Wang PW, Yang SC, Chou WL, Fang JY. Cosmetic and Therapeutic Applications of Fish Oil's Fatty Acids on the Skin. Mar Drugs. 2018;16(8):256. DOI: 10.3390/md16080256; PMCID: PMC6117694; PMID: 30061538
19. Rinawati R, Agustina R, Suhartono E. Penyembuhan luka dengan penurunan eritema pada tikus putih (Rattus norvegicus) yang diberi getah batang jarak cina (Jatropha multifida L). Dunia Keperawatan J Keperawatan Kesehatan. 2015;3(1):1-11.
20. Divadi A, Yuliani SH. Pembuatan dan Uji Aktivitas Sediaan Gel Scarless Wound dengan Ekstrak Binahong dan Zat Aktif Piroxicam. J Pharm Sci Commun. 2016;12(2):41-7. DOI: 10.24071/jpsc.122130
21. Rahmanda A. Uji Efek Penyembuhan Luka Fase Minyak Ekstrak Ikan Toman (Channa micropeltes) pada Tikus Putih Jantan Wistar yang Diberi Luka Sayat. J Mahasiswa Farmasi Fakultas Kedokteran UNTAN. 2014;1(1):1-11.
22. Moro J, Tomé D, Schmidely P, Demersay TC, Azzout-Marniche D. Histidine: A Systematic Review on Metabolism and Physiological Effects in Human and Different Animal Species. Nutrients. 2020;12(5):1414. DOI: 10.3390/nu12051414; PMCID: PMC7284872; PMID: 32423010
23. Petraru A, Amariei S. Rapeseed-An Important Oleaginous Plant in the Oil Industry and the Resulting Meal a Valuable Source of Bioactive Compounds. Plants. 2024;13(21):3085. DOI: 10.3390/plants13213085; PMCID: PMC11548519; PMID: 39520003
24. Nurfaidah, Asikin AN, Kasmiati, Angraeni. Amino acid profile and potential utilization purposes of albumin from four types of freshwater fish in Makassar, South Sulawesi, Indonesia. Biodiversitas. 2024;25(11):4199-207. DOI: 10.13057/biodiv/d251119
25. Torsabo D, Ishak SD, Noordin NM, Waiho K, Koh ICC, Yazed MA, et al. Optimizing reproductive performance in pangasius catfish broodstock: A review of dietary and molecular strategies. Vet Anim Sci. 2024;25:100375. DOI: 10.1016/j.vas.2024.100375; PMCID: PMC11245938; PMID: 39005967
26. Mittendorfer B, Volpi E, Wolfe RR. Whole body and skeletal muscle glutamine metabolism in healthy subjects. Am J Physiol Endocrinol Metab. 2001;280(2):E23-33. DOI: 10.1152/ajpendo.2001.280.2.e323; PMCID: PMC3425386; PMID: 11158937
27. Walker MC, van der Donk WA. The many roles of glutamate in metabolism. J Ind Microbiol Biotechnol. 2016;43(2-3):419-30. DOI: 10.1007/s10295-015-1665-y; PMCID: PMC4753154; PMID: 26323613
28. Boutard V, Fouqueray B, Philippe C, Perez J, Baud L. Fish oil supplementation and essential fatty acid deficiency reduce nitric oxide synthesis by rat macrophages. Kidney Int. 1994;46(5):1280-6. DOI: 10.1038/ki.1994.395; PMID: 7531789
29. Zhao Z, Wang Y, Li Q, Zhao H, Duan Y, Wu X, et al. Effects of the photovoltaic fishery culture model on muscle nutritional quality and volatile flavor compounds of Litopenaeus vannamei. Heliyon. 2024;10(15):e34797. DOI: 10.1016/j.heliyon.2024.e34797; PMCID: PMC11332832; PMID: 39161840
30. Gambardella J, Khonkar W, Morelli MB, Wang X, Santulli G, Trimarco V. Arginine and Endothelial Function. Biomedicines. 2020;8(8):277. DOI: 10.3390/biomedicines8080277; PMCID: PMC7460461; PMID: 32781796
31. Gornik HL, Creager MA. Arginine and endothelial and vascular health. J Nutr. 2004;134(10 Suppl):2880-S-7S. DOI: 10.1093/jn/134.10.2880s; PMID: 15465805
32. Langendörfer LJ, Avdylaj B, Hensel O, Diakité D. Design of Plant-Based Food: Influences of Macronutrients and Amino Acid Composition on the Techno-Functional Properties of Legume Proteins. 2023;12(20):3787. DOI: 10.3390/foods12203787; PMCID: PMC10606351; PMID: 37893680
33. Wu G, Meininger CJ, McNeal CJ, Bazer FW, Rhoads JM. Role of L-Arginine in Nitric Oxide Synthesis and Health in Humans. Adv Exp Med Biol. 2021;1332:167-87. DOI: 10.1007/978-3-030-74180-8_10; PMID: 34251644
34. Barbul A, Lazarou SA, Efron DT, Wasserkrug HL, Efron G. Arginine enhances wound healing and lymphocyte immune responses in humans. Surgery. 1990;108(2):331-6. PMID: 2382229
35. Landén NX, Li D, Ståhle M. Transition from inflammation to proliferation: a critical step during wound healing. Cell Mol Life Sci. 2016;73(20):3861-85. DOI: 10.1007/s00018-016-2268-0; PMCID: PMC5021733; PMID: 27180275
36. Segalla GV, Teixeira ST, Rogero MM. Nutritional therapy and wound healing in pressure injury situations: an integrative review. Nutrire. 2021;46:21. DOI: 10.1186/s41110-021-00147-3
37. Ikhsan AN, Irnawati I, Lestari LA, Erwanto Y, Rohman A. Simultaneous analysis of patin fish oil (Pangasius micronemus) and bandeng (Chanos chanos) fish oil using FTIR spectroscopy and chemometrics. Food Res. 2022;6(3):262-8. DOI: 10.26656/fr.2017.6(3).353
38. Lei XX, Cheng LHH, Lin HY, Yang Y, Lu YY, Pang MR, et al. The minimal active domain of human salivary histatin 1 is efficacious in promoting acute skin wound healing. Mil Med Res. 2022;9(1):41. DOI: 10.1186/s40779-022-00398-9; PMCID: PMC9287874; PMID: 35841072
39. Murakami H, Shimbo K, Inoue Y, Takino Y, Kobayashi H. Importance of amino acid composition to improve skin collagen protein synthesis rates in UV-irradiated mice. Amino Acids. 2012;42(6):2481-9. DOI: 10.1007/s00726-011-1059-z; PMCID: PMC3351609; PMID: 21861170
40. Lim JM, Kim G, Levine RL. Methionine in Proteins: It's Not Just for Protein Initiation Anymore. Neurochem Res. 2019;44(1):247-57. DOI: 10.1007/s11064-017-2460-0; PMCID: PMC6446232; PMID: 29327308
41. Holeček M. Histidine in Health and Disease: Metabolism, Physiological Importance, and Use as a Supplement. Nutrients. 2020;12(3):848. DOI: 10.3390/nu12030848; PMCID: PMC7146355; PMID: 32235743
42. Sudha C, Ahilan B, Felix N, Uma A, Chidambaram P, Prabu E. Replacement of fish oil with black soldier fly larvae oil and vegetable oils: Effects of growth, whole-body fatty acid profile, digestive enzyme activity, haemato-biochemical responses and muscle growth-related gene expression of juvenile striped catfish, Pangasianodon hypophthalmus. Aquac Res. 2022;53(8):3097-111. DOI: 10.1111/are.15823
43. Hwang W, Lei W, Katritsis NM, MacMahon M, Chapman K, Han N. Current and prospective computational approaches and challenges for developing COVID-19 vaccines. Adv Drug Deliv Rev. 2021;172:249-74. DOI: 10.1016/j.addr.2021.02.004; PMCID: PMC7871111; PMID: 33561453
44. Tardy AL, Pouteau E, Marquez D, Yilmaz C, Scholey A. Vitamins and Minerals for Energy, Fatigue and Cognition: A Narrative Review of the Biochemical and Clinical Evidence. Nutrients. 2020;12(1):228. DOI: 10.3390/nu12010228; PMCID: PMC7019700; PMID: 31963141
Authors
1.
Hidayaturrahmah H, Suprayogi A, Hanif N, Roosita K, Darusman HS, Aprilyana L. Analysis of Amino Acid Profiles in Bone, Oil, and Muscle Tissue and Wound Healing Activity of Pangasius hypophthalmus Oil in Rattus norvegicus. Borneo J Pharm [Internet]. 2025Feb.28 [cited 2025May1];8(1):95-106. Available from: https://journal.umpr.ac.id/index.php/bjop/article/view/8182
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