Iranian Journal of Veterinary Surgery

Iranian Journal of Veterinary Surgery

Evaluation of Protective Effects of Pomegranate Seed Oil on Experimental Osteoporosis in Rats

Document Type : Original Article

Authors
Farzaneh Khodadadi 1
Zahra Moosavi 2
Soheil Sadr 1
Ali Mirshahi 3
Hossein Kazemi Mehrjerdi 3
1 Graduated student, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.
2 Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.
3 Department of Clinical Sciences, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran.
10.30500/ivsa.2023.422083.1371
Abstract
Osteoporosis is characterized by a reduction of bone mass and destruction of bone structures, followed by high bone fragility and susceptibility. This study aims to evaluate the protective effects of pomegranate seed oil (PSO) on experimental osteoporosis in rats. Twenty-four female Wistar rats were divided into four groups: sham-operated (Sham = 6), Sham with PSO treatment (Sham+PSO = 6), ovariectomized (OVX = 6), and ovariectomized with PSO treatment (OVX+PSO = 6). OVX+PSO and Sham+PSO groups received 0.1 ml of pomegranate juice daily, and OVX and Sham groups received the same amount of paraffin oil. After eight weeks, the femur and tibia bones were removed, and the structure and metabolism of samples were assessed by histological examination. The average thickness of femoral neck trabeculae in group OVX was significantly lower than in groups Sham+PSO and Sham (p < 0.05). Regarding the number of trabeculae in the neck of the femur, a significant difference was observed between groups OVX and Sham+PSO (p < 0.05). Furthermore, trabecular separation in group OVX was significantly more than in the other three groups (p < 0.05). The trabecular separation in group OVX+PSO compared to groups Sham+PSO and Sham was significantly higher (p < 0.05). A histopathologic examination of the upper metaphysis of the tibia indicated that the number of bone trabeculae in Sham+PSO was only statistically significant in the OVX group (p = 0.018). It was also found that the average thickness of bone trabeculae in the OVX+PSO and Sham groups was significantly lower than in the Sham+SO group. The results of the present study suggest that pomegranate seed oil, having estrogenic compounds, can prevent osteoporosis in rats caused by ovariectomy.
Keywords
Estradiol
Histopathology
Osteoporosis
Pomegranate
Subjects
  1. Wani IM, Arora S. Computer-aided diagnosis systems for osteoporosis detection: A comprehensive survey. Medical and Biological Engineering and Computing. 2020; 58(9): 1873-1917.
  2. Mazziotti G, Lania AG, Canalis E. Skeletal disorders associated with the growth hormone–insulin-like growth factor 1 axis. Nature Reviews Endocrinology. 2022; 18(6): 353-365.
  3. Al Anouti F, Taha Z, Shamim S, Khalaf K, Al Kaabi L, Alsafar H. An insight into the paradigms of osteoporosis: From genetics to biomechanics. Bone Reports. 2019; 11: 100216.
  4. Li S, Mao Y, Zhou F, Yang H, Shi Q, Meng B. Gut microbiome and osteoporosis: A review. Bone and Joint Research. 2020; 9(8): 524-530.
  5. Rolvien T, Amling M. Disuse osteoporosis: clinical and mechanistic insights. Calcified Tissue International. 2022; 110(5): 592-604.
  6. Carina V, Della Bella E, Costa V, Bellavia D, Veronesi F, Cepollaro S, Fini M. Bone's response to mechanical loading in aging and osteoporosis: Molecular mechanisms. Calcified Tissue International. 2020; 107(4): 301-318.
  7. Aibar-Almazán A, Voltes-Martínez A, Castellote-Caballero Y, Afanador-Restrepo DF, Carcelén-Fraile MdC, López-Ruiz E. Current status of the diagnosis and management of osteoporosis. International Journal of Molecular Sciences. 2022; 23(16): 9465.
  8. Mazziotti G, Formenti AM, Adler RA, Bilezikian JP, Grossman A, Sbardella E, Minisola S, Giustina A. Glucocorticoid-induced osteoporosis: pathophysiological role of GH/IGF-I and PTH/Vitamin D axes, treatment options and guidelines. Endocrine. 2016; 54(3): 603-611.
  9. Lata PF, Elliott ME. Patient assessment in the diagnosis, prevention, and treatment of osteoporosis. Nutrition in Clinical Practice. 2007; 22(3): 261-275.
  10. Gatti D, Fassio A. Pharmacological management of osteoporosis in postmenopausal women: the current state of the art. Journal of Population Therapeutics and Clinical Pharmacology. 2019; 26(4): e1-e17.
  11. Shroff R, Fewtrell M, Heuser A, Kolevica A, Lalayiannis A, McAlister L, Silva S, Goodman N, Schmitt CP, Biassoni L, Rahn A, Fischer DC, Eisenhauer A. Naturally occurring stable calcium isotope ratios in body compartments provide a novel biomarker of bone mineral balance in children and young adults. Journal of Bone and Mineral Research. 2021; 36(1): 133-142.
  12. Bhattarai HK, Shrestha S, Rokka K, Shakya R. Vitamin D, calcium, parathyroid hormone, and sex steroids in bone health and effects of aging. Journal of Osteoporosis. 2020; 9324505.
  13. Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocrine Reviews. 2010; 31(3): 266-300.
  14. Demontiero O, Vidal C, Duque G. Aging and bone loss: new insights for the clinician. Therapeutic Advances in Musculoskeletal Disease. 2012; 4(2): 61-76.
  15. Yang S, Center J, Eisman J, Nguyen T. Association between fat mass, lean mass, and bone loss: the Dubbo Osteoporosis Epidemiology Study. Osteoporosis International. 2015; 26(4): 1381-1386.
  16. Wu S-F, Du X-J. Body mass index may positively correlate with bone mineral density of lumbar vertebra and femoral neck in postmenopausal females. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research. 2016; 22: 145-151.
  17. Kendler DL, Bauer DC, Davison KS, Dian L, Hanley DA, Harris S, McClung MR, Miller PD, Schousboe JT, Tuen CK, Lewiecki EM. Vertebral fractures: clinical importance and management. The American Journal of Medicine. 2016; 129(2): 221.e1-221.e10.
  18. Tai V, Leung W, Grey A, Reid IR, Bolland MJ. Calcium intake and bone mineral density: systematic review and meta-analysis. BMJ. 2015; 351.
  19. Lorentzon M, Cummings SR. Osteoporosis: the evolution of a diagnosis. Journal of Internal Medicine. 2015; 277(6): 650-661.
  20. Choksi P, Jepsen KJ, Clines GA. The challenges of diagnosing osteoporosis and the limitations of currently available tools. Clinical Diabetes and Endocrinology. 2018; 4(1): 1-13.
  21. Shirzadfar H, Gordoghli N. A Comparative study of current methods and recent advances in the diagnosis and assessment of osteoporosis. Recent Research in Endocrinology and Metabolic Disorder. 2020; 2(1): 3-17.
  22. Raterman HG, Bultink IE, Lems WF. Osteoporosis in patients with rheumatoid arthritis: an update in epidemiology, pathogenesis, and fracture prevention. Expert Opinion on Pharmacotherapy. 2020; 21(14): 1725-1737.
  23. Fardellone P, Salawati E, Le Monnier L, Goëb V. Bone loss, osteoporosis, and fractures in patients with rheumatoid arthritis: a review. Journal of Clinical Medicine. 2020; 9(10): 3361.
  24. Hoenig T, Ackerman KE, Beck BR, Bouxsein ML, Burr DB, Hollander K, Popp KL, Rolvien T, Tenforde AS, Warden SJ. Bone stress injuries. Nature Reviews Disease Primers. 2022; 8(1): 1-20.
  25. Chen S, Lin Y, Li S, Ye Y, Xie L, Chen J, Wu H, Cheng Y, Ge J. Comparison of bone histomorphology and bone mineral density in different parts of ovariectomized osteoporosis rats. Journal of Hard Tissue Biology. 2019; 28(2): 199-206.
  26. Ma YL, Burr DB, Erben RG. Bone histomorphometry in rodents. In: Bilezikian JP, Martin TJ, Clemens TL, Rosen CJ, eds. Principles of Bone Biology. 4th Elsevier, 2020; 1899-1922.
  27. Kim J-Y, Cheon Y-H, Yoon K-H, Lee MS, Oh J. Parthenolide inhibits osteoclast differentiation and bone resorbing activity by down-regulation of NFATc1 induction and c-Fos stability, during RANKL-mediated osteoclastogenesis. BMB Reports. 2014; 47(8): 451.
  28. Ceccarelli I, Bioletti L, Peparini S, Solomita E, Ricci C, Casini I, Miceli E, Aloisi AM. Estrogens and phytoestrogens in body functions. Neuroscience and Biobehavioral Reviews. 2022; 132: 648-663.
  29. Kumari A, Dora J, Kumar A, Kumar A. Pomegranate (Punica granatum)—overview. International Journal of Pharmaceutical and Chemical Sciences. 2012; 1(4): 1218-1222.
  30. Mahesar SA, Kori AH, Sherazi STH, Kandhro AA, Laghari ZH. Pomegranate (Punica granatum) seed oil. In: Ramadan MF, ed. Fruit Oils: Chemistry and Functionality. Springer, 2019; 691-709.
  31. Zielińska A, Wójcicki K, Klensporf-Pawlik D, Marzec M, Lucarini M, Durazzo A, Fonseca J, Santini A, Nowak I, Souto ES. Cold-pressed pomegranate seed oil: Study of punicic acid properties by coupling of GC/FID and FTIR. 2022; 27(18): 5863.
  32. Venkitasamy C, Zhao L, Zhang R, Pan Z. Pomegranate. Integrated Processing Technologies for Food and Agricultural By-Products. Elsevier, 2019; 181-216.
  33. Hamouda AF, Shaban NZ. Short and long term effects of pomegranate (Punica granatum) extracts on apoptosis in rat kidney induced by diethylnitrosamine and phenobarbital. Journal of Pharmacy and Pharmacology.2016; 4(2): 52-63.
  34. Kim ND, Mehta R, Yu W, Neeman I, Livney T, Amichay A, Poirier D, Nicholls P, Kirby A, Jiang W, Mansel R, Ramachandran C, Rabi T, Kaplan B, Lansky E. Chemopreventive and adjuvant therapeutic potential of pomegranate (Punica granatum) for human breast cancer. Breast Cancer Research and Treatment. 2002; 71(3): 203-217.
  35. Newman RA, Lansky EP, Block ML, eds. Pomegranate: The Most Medicinal Fruit. 1st Basic Health Publications, Inc. 2007.
  36. Zarfeshany A, Asgary S, Javanmard SH. Potent health effects of pomegranate. Advanced Biomedical Research. 2014; 3: 100.
  37. Montenegro L. Nanocarriers for skin delivery of cosmetic antioxidants. Journal of Pharmacy and Pharmacognosy Research. 2014; 2(4): 73-92.
  38. Li C, Liang B, Shi X, Wang H. Opg/Rankl mRNA dynamic expression in the bone tissue of ovariectomized rats with osteoporosis. Genetics and Molecular Research. 2015; 14(3): 9215-9224.
  39. Johnston BD, Ward WE. The ovariectomized rat as a model for studying alveolar bone loss in postmenopausal women. BioMed Research International. 2015; 635023
  40. Kimmel DB. Animal models for in vivo experimentation in osteoporosis research. In: Marcus R, Feldman D, Kelsey J, eds. Osteoporosis. 2nd edn. Elsevier, 2001; 29-47.
  41. Fischer V, Haffner-Luntzer M. Interaction between bone and immune cells: Implications for postmenopausal osteoporosis. Seminars in Cell and Developmental Biology. 2022; 123: 14-21.
  42. Hassan HA, El Wakf AM, El Gharib NE. Role of phytoestrogenic oils in alleviating osteoporosis associated with ovariectomy in rats. Cytotechnology. 2013; 65(4): 609-619.
  43. Mattia C, Coluzzi F, Celidonio L, Vellucci R. Bone pain mechanism in osteoporosis: a narrative review. Clinical Cases in Mineral and Bone Metabolism. 2016; 13(2): 97-100.
  44. Wehrle-Martinez A, Lawrence K, Back PJ, Rogers CW, Gibson M, Dittmer KE. Osteoporosis is the cause of spontaneous humeral fracture in dairy cows from New Zealand. Veterinary Pathology. 2023; 60(1): 88-100.
  45. Oliveira GR, Vargas-Sanchez PK, Fernandes RR, Ricoldi MST, Semeghini MS, Pitol DL, de Sousa LG, Siessere S, Bombonato-prado KF. Lycopene influences osteoblast functional activity and prevents femur bone loss in female rats submitted to an experimental model of osteoporosis. Journal of Bone and Mineral Metabolism. 2019; 37(4): 658-667.
  46. Sequeira L, Nguyen J, Wang L, Nohe A. A Novel Peptide, CK2. 3, Improved bone formation in ovariectomized sprague dawley rats. International Journal of Molecular Sciences. 2020; 21(14): 4874.
  47. Yamamoto N, Jee WS, Ma YF. Bone histomorphometric changes in the femoral neck of aging and ovariectomized rats. The Anatomical Record. 1995; 243(2): 175-185.
  48. Li M, Shen Y, Wronski T. Time course of femoral neck osteopenia in ovariectomized rats. Bone. 1997; 20(1): 55-61.
  49. Chiba H, Uehara M, Wu J, Wang X, Masuyama R, Suzuki K, Kanazawa K, Ishimi Y. Hesperidin, a citrus flavonoid, inhibits bone loss and decreases serum and hepatic lipids in ovariectomized mice. Journal of Nutrition. 2003;133(6): 1892-1897.
  50. Wang X, Wu J, Chiba H, Umegaki K, Yamada K, Ishimi Y. Puerariae radix prevents bone loss in ovariectomized mice. Journal of Bone and Mineral Metabolism. 2003; 21(5): 268-275.
  51. Monsefi M, Parvin F, Talaei-Khozani T. Effects of pomegranate extracts on cartilage, bone and mesenchymal cells of mouse fetuses. British Journal of Nutrition. 2012; 107(5): 683-690.
  52. Mori-Okamoto J, Otawara-Hamamoto Y, Yamato H, Yoshimura H. Pomegranate extract improves a depressive state and bone properties in menopausal syndrome model ovariectomized mice. Journal of Ethnopharmacology. 2004; 92(1): 93-101.
  53. Peng S, Xia R, Fang H, Li F, Chen A, Zhang G, Qin L. Effect of epimedium-derived phytoestrogen on bone turnover and bone microarchitecture in OVX-induced osteoporotic rats. Journal of Huazhong University of Science and Technology [Medical Sciences]. 2008 ;28(2): 167-170.
  54. Yao W, Hadi T, Jiang Y, Lotz J, Wronski TJ, Lane NE. Basic fibroblast growth factor improves trabecular bone connectivity and bone strength in the lumbar vertebral body of osteopenic rats. Osteoporosis International. 2005; 16(12): 1939-1947.

  • Receive Date 23 October 2023
  • Revise Date 14 November 2023
  • Accept Date 16 December 2023
  • First Publish Date 16 December 2023