J Nutr Health.  2019 Aug;52(4):323-331. 10.4163/jnh.2019.52.4.323.

Protective effect of dietary oils containing omega-3 fatty acids against glucocorticoid-induced osteoporosis

Affiliations
  • 1Department of Bioecology, Hygiene and public health, Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, 420012, Russia. amelbahnasavi@stud.kpfu.ru
  • 2Department of Nutrition and Food Sciences, National Research Centre, Dokki, Giza, 12622, Egypt.

Abstract

PURPOSE
Glucocorticoids (GCs) are implicated in secondary osteoporosis, and the resulting fractures cause significant morbidity. Polyunsaturated fatty acids (PUFAs) play a vital role in bone metabolism. However, few trials have studied the impact of omega-3 PUFA-containing oils against GC-induced osteoporosis. Therefore, the present study was undertaken to determine whether supplementation with omega-3 PUFA-containing dietary oils such as fish oil, flaxseed oil or soybean oil can impede the development of GC-induced osteoporosis.
METHODS
The fatty acids (FAs) content of oils was determined using gas chromatography. Male rats were subdivided into 5 groups (8 rats each): normal control (balanced diet), prednisolone control (10 mg/kg prednisolone daily), soybean oil (prednisolone 10 mg/kg + soybean oil 7% w/w), flaxseed oil (prednisolone 10 mg/kg + flaxseed oil 7% w/w), and fish oil (from cod liver; prednisolone 10 mg/kg + fish oil 7% w/w).
RESULTS
The study data exhibited a significant depletion in bone mineral density (BMD) and femur mass in the prednisolone control compared to the normal control, accompanied with a marked decrease in the levels of plasma calcium and 1,25-(OH)₂-vitamin D₃, and elevated levels of C-terminal telopeptide (CTX), tumor necrosis factor-alpha (TNF-α) and malondialdehyde (MDA). Supplementation with fish oil, soybean oil or flaxseed oil helped to improve plasma calcium levels, and suppress oxidative stress and inflammatory markers. Additionally, bone resorption was suppressed as reflected by the decreased CTX levels. However, fish oil was more effective than the other two oils with a significant improvement in BMD and normal histological results compared to the normal control.
CONCLUSION
This study demonstrated that supplementation with dietary oils containing omega-3 PUFAs such as fish oil, soybean oil or flaxseed oil can play a role in the prevention of bone loss and in the regulation of bone metabolism, especially fish oil which demonstrated a greater level of protection against GC-induced osteoporosis.

Keyword

glucocorticoid-induced osteoporosis; fish oil; soybean oil; flaxseed oil; inflammation

MeSH Terms

Animals
Bone Density
Bone Resorption
Calcium
Chromatography, Gas
Dietary Fats, Unsaturated*
Fatty Acids
Fatty Acids, Omega-3*
Fatty Acids, Unsaturated
Femur
Fish Oils
Glucocorticoids
Humans
Inflammation
Linseed Oil
Liver
Male
Malondialdehyde
Metabolism
Oils
Osteoporosis*
Oxidative Stress
Plasma
Prednisolone
Rats
Soybean Oil
Tumor Necrosis Factor-alpha
Calcium
Dietary Fats, Unsaturated
Fatty Acids
Fatty Acids, Omega-3
Fatty Acids, Unsaturated
Fish Oils
Glucocorticoids
Linseed Oil
Malondialdehyde
Oils
Prednisolone
Soybean Oil
Tumor Necrosis Factor-alpha

Figure

  • Fig. 1 Photomicrographs of bones of rats from (A) the normal control group showing no histopathological changes, normal cortical bone thickness and normal osteocyte; (B) the prednisolone control group showing several resorption cavities within the matrix, abnormal osteocyte, and thin cortical bone with presence of cracks and fissures; (C) the soybean oil group (S) showing few cracks and fissures in the cortical bone; (D) the flaxseed oil group (X) showing focal necrosis with few cracks and fissures in the cortical bone; and (E) the fish oil group (F) showing no histopathological changes, normal bone cortex and normal osteocyte (H & E × 100).


Reference

1. Jeremiah MP, Unwin BK, Greenawald MH, Casiano VE. Diagnosis and management of osteoporosis. Am Fam Physician. 2015; 92(4):261–268.
2. Akarirmak U. Osteoporosis: a major problem - worldwide. Arch Sports Med. 2018; 2(1):106–108.
Article
3. Wade SW, Strader C, Fitzpatrick LA, Anthony MS, O'Malley CD. Estimating prevalence of osteoporosis: examples from industrialized countries. Arch Osteoporos. 2014; 9(1):182.
Article
4. Silverman S, Curtis J, Saag K, Flahive J, Adachi J, Anderson F, et al. International management of bone health in glucocorticoid-exposed individuals in the observational GLOW study. Osteoporos Int. 2015; 26(1):419–420.
Article
5. Wang T, Yu X, He C. Pro-inflammatory cytokines: cellular and molecular drug targets for glucocorticoid-induced-osteoporosis via osteocyte. Curr Drug Targets. 2019; 20(1):1–15.
Article
6. Compston J. Glucocorticoid-induced osteoporosis: an update. Endocrine. 2018; 61(1):7–16.
Article
7. Lavado-García J, Roncero-Martin R, Moran JM, Pedrera-Canal M, Aliaga I, Leal-Hernandez O, et al. Long-chain omega-3 polyunsaturated fatty acid dietary intake is positively associated with bone mineral density in normal and osteopenic Spanish women. PLoS One. 2018; 13(1):e0190539.
Article
8. Kelly OJ, Gilman JC, Kim Y, Ilich JZ. Long-chain polyunsaturated fatty acids may mutually benefit both obesity and osteoporosis. Nutr Res. 2013; 33(7):521–533.
Article
9. Iolascon G, Gimigliano R, Bianco M, De Sire A, Moretti A, Giusti A, et al. Are dietary supplements and nutraceuticals effective for musculoskeletal health and cognitive function? A scoping review. J Nutr Health Aging. 2017; 21(5):527–538.
Article
10. Hutchins-Wiese HL, Picho K, Watkins BA, Li Y, Tannenbaum S, Claffey K, et al. High-dose eicosapentaenoic acid and docosahexaenoic acid supplementation reduces bone resorption in postmenopausal breast cancer survivors on aromatase inhibitors: a pilot study. Nutr Cancer. 2014; 66(1):68–76.
Article
11. El-Saeed GS, Elghoroury EA, Morsy S, Aly HM, Wafaey H. Phenotype of vitamin D receptor gene polymorphisms, impact of feeding flaxseed oil, and osteoporosis in ovariectomized diabetic rats. Bull Natl Res Cent. 2018; 42(1):11.
Article
12. 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.
Article
13. American Oil Chemists' Society (AOCS). Official methods and recommended practices of the AOCS. Champaign (IL): AOCS;2009.
14. Veronezi CM, Costa T, Jorge N. Basil (Ocimum Basilicum L.) as a natural antioxidant. J Food Process Preserv. 2014; 38(1):255–261.
15. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123(11):1939–1951.
Article
16. Kaczmarczyk-Sedlak I, Zych M, Rotko K, Sedlak L. Effects of thalidomide on the development of bone damage caused by prednisolone in rats. Pharmacol Rep. 2012; 64(2):386–395.
17. Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990; 186:421–431.
18. Bancroft JD, Gamble M. Theory and practice of histological techniques. 5th edition. London: Churchill Livingstone;2002.
19. Le HT, Phi LT, Dao TT, Phan NK, Van Pham P, Vu NB. A mouse model of osteonecrotic femoral head induced by methylprednisolone and lipopolysaccharide. Biomedical Research and Therapy. 2016; 3(3):548–556.
Article
20. Ton FN, Gunawardene SC, Lee H, Neer RM. Effects of low-dose prednisone on bone metabolism. J Bone Miner Res. 2005; 20(3):464–470.
Article
21. Kaczmarczyk-Sedlak I, Cegieła U, Nowińska B, Folwarczna J. Effects of catecholamines on the intramedullary pressure in the femur in rats with prednisolone-induced osteoporosis. Pharmacol Rep. 2006; 58(4):540–550.
22. Lau BY, Cohen DJ, Ward WE, Ma DW. Investigating the role of polyunsaturated fatty acids in bone development using animal models. Molecules. 2013; 18(11):14203–14227.
Article
23. Watkins BA, Li Y, Lippman HE, Feng S. Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism. Prostaglandins Leukot Essent Fatty Acids. 2003; 68(6):387–398.
Article
24. Bullon P, Battino M, Varela-Lopez A, Perez-Lopez P, Granados-Principal S, Ramirez-Tortosa MC, et al. Diets based on virgin olive oil or fish oil but not on sunflower oil prevent age-related alveolar bone resorption by mitochondrial-related mechanisms. PLoS One. 2013; 8(9):e74234.
Article
25. Antonacci LE, Bussetti M, Rodriguez MA, Cano AV, Gagliostro GA. Effect of diet supplementation with combinations of soybean and linseed oils on milk production and fatty acid profile in lactating dairy ewes. Agric Sci. 2018; 9(2):200–220.
26. Dorni C, Sharma P, Saikia G, Longvah T. Fatty acid profile of edible oils and fats consumed in India. Food Chem. 2018; 238:9–15.
Article
27. Calder PC. Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance. Biochim Biophys Acta. 2015; 1851(4):469–484.
Article
28. Shah SK, Gecys GT. Prednisone-induced osteoporosis: an overlooked and undertreated adverse effect. J Am Osteopath Assoc. 2006; 106(11):653–657.
29. Pennisi P, D'Alcamo MA, Leonetti C, Clementi A, Cutuli VM, Riccobene S, et al. Supplementation of L-arginine prevents glucocorticoid-induced reduction of bone growth and bone turnover abnormalities in a growing rat model. J Bone Miner Metab. 2005; 23(2):134–139.
Article
30. Lukas R, Gigliotti JC, Smith BJ, Altman S, Tou JC. Consumption of different sources of omega-3 polyunsaturated fatty acids by growing female rats affects long bone mass and microarchitecture. Bone. 2011; 49(3):455–462.
Article
31. Sun L, Tamaki H, Ishimaru T, Teruya T, Ohta Y, Katsuyama N, et al. Inhibition of osteoporosis due to restricted food intake by the fish oils DHA and EPA and perilla oil in the rat. Biosci Biotechnol Biochem. 2004; 68(12):2613–2615.
Article
32. Mazziotti G, Formenti AM, Adler RA, Bilezikian JP, Grossman A, Sbardella E, et al. Glucocorticoid-induced osteoporosis: pathophysiological role of GH/IGF-I and PTH/VITAMIN D axes, treatment options and guidelines. Endocrine. 2016; 54(3):603–611.
Article
33. Suarez-Bregua P, Guerreiro PM, Rotllant J. Stress, glucocorticoids and bone: a review from mammals and fish. Front Endocrinol (Lausanne). 2018; 9:526.
Article
34. Heaney RP, Carey R, Harkness L. Roles of vitamin D, n-3 polyunsaturated fatty acid, and soy isoflavones in bone health. J Am Diet Assoc. 2005; 105(11):1700–1702.
Article
35. Maditz KH, Smith BJ, Miller M, Oldaker C, Tou JC. Feeding soy protein isolate and oils rich in omega-3 polyunsaturated fatty acids affected mineral balance, but not bone in a rat model of autosomal recessive polycystic kidney disease. BMC Nephrol. 2015; 16(1):13.
Article
36. Jaafarnejad F, Hosseini SF, Mazlom SR, Hami M. Comparison of the effect of fish oil and vitamin E on the duration of Cyclic mastalgia. Evid Based Care J. 2013; 3(1):69–76.
37. An WS, Lee SM, Son YK, Kim SE, Kim KH, Han JY, et al. Omega-3 fatty acid supplementation increases 1,25-dihydroxyvitamin D and fetuin-A levels in dialysis patients. Nutr Res. 2012; 32(7):495–502.
Article
38. Lee SM, Son YK, Kim SE, An WS. The effects of omega-3 fatty acid on vitamin D activation in hemodialysis patients: a pilot study. Mar Drugs. 2015; 13(2):741–755.
Article
39. Dong H, Hutchins-Wiese H, Kleppinger A, Annis K, Liva E, Lammi-Keefe C, et al. Effects of omega-3 polyunsaturated fatty acid supplementation on bone turnover in older women. Int J Vitam Nutr Res. 2014; 84(3-4):124–132.
Article
40. Varela-López A, Ochoa JJ, Llamas-Elvira JM, López-Frías M, Planells E, Speranza L, et al. Loss of bone mineral density associated with age in male rats fed on sunflower oil is avoided by virgin olive oil intake or coenzyme Q supplementation. Int J Mol Sci. 2017; 18(7):E1397.
Article
41. Chen AB, Minami K, Raposo JF, Matsuura N, Koizumi M, Yokota H, et al. Transient modulation of calcium and parathyroid hormone stimulates bone formation. Endocrine. 2016; 54(1):232–240.
Article
42. Han H, Qiu F, Zhao H, Tang H, Li X, Shi D. Dietary flaxseed oil prevents western-type diet-induced nonalcoholic fatty liver disease in apolipoprotein-E knockout mice. Oxid Med Cell Longev. 2017; 2017:3256241.
Article
43. Klein K, Gay S. Epigenetics in rheumatoid arthritis. Curr Opin Rheumatol. 2015; 27(1):76–82.
Article
44. Muga MA, Chao JC. Effects of fish oil and spirulina on oxidative stress and inflammation in hypercholesterolemic hamsters. BMC Complement Altern Med. 2014; 14(1):470.
Article
45. Pipingas A, Sinclair A, Croft KD, Januszewski AS, Jenkins AJ, Mori TA, et al. Fish oil and multivitamin supplementation reduces oxidative stress but not inflammation in healthy older adults: a randomised controlled trial. J Funct Foods. 2015; 19:949–957.
Article
46. Kasem MA, Khedr ES, Abdel-Aleem AM, Said AS. Histological effect of bisphosphonate, vitamin D and olive oil on glucocorticoid induced osteoporosis (Gio) in Albino Rat. Egypt J Hosp Med. 2016; 65:699–708.
Article
47. Derakhshanian H, Djalali M, Djazayery A, Nourijelyani K, Ghadbeigi S, Pishva H, et al. Quercetin prevents experimental glucocorticoid-induced osteoporosis: a comparative study with alendronate. Can J Physiol Pharmacol. 2013; 91(5):380–385.
Article
48. Liu D, Veit HP, Wilson JH, Denbow DM. Long-term supplementation of various dietary lipids alters bone mineral content, mechanical properties and histological characteristics of Japanese quail. Poult Sci. 2003; 82(5):831–839.
Article
Full Text Links
  • JNH
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr