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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2021; 67(2): 67-75


EFFECT OF OBESITY ON BONE METABOLISM

I.G. Litovka

    O.O. Bogomolets Institute of Physiology of the National Academy of Sciences of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz67.02.067

Abstract

The review of current literature presents data on the prevalence of obesity and its impact on bone metabolism. These results suggest that there is a complex multilevel relationship between the skeletal system, adipose tissue and energy metabolism. However, informational analysis of the problem has shown that there are still many unresolved issues regarding the relationship between metabolic and osteopenic syndromes. At the same time, studies of the state of the skeletal system in metabolic syndrome and obesity can contribute to a deeper understanding of the pathogenesis of osteopenic syndrome to develop its treatment and prevention.

Keywords: obesity; bone metabolic; source tissue

References

  1. World health organization global health observatory. Obesity: situation and trends, 2017. Available from http:// www.who.int/gho/ncd/risk_factors/obesity_text/en.
  2. European Association for the study of obesity. Facts & Statistics: Definitions of overweight and obese, 2017. Available from http://easo.org/task-forces/childhoodobesity-cotf/facts-statistics/.
  3. Shapses SA, Pop CL, Wang Y. Obesity is a concern for bone health with aging. Nutr Res. 2017;39:1-13. CrossRef PubMed PubMedCentral
  4. Misyura EV, Kazakov AV, Kravchun NA. Epidemiological aspects of obesity in Ukraine. Endocrinology. 2014;19 (4):3-25.[Russian].
  5. Ginzburg MM, Kozupitsa GS. Insulin resistance syndrome. Endocrsnol Probl. 1997;43(1):40-3. [Rusian]. CrossRef
  6. Grigoryan OR, Chernova TO, Antsiferov MB. Correction of insulin resistance in postmenopausal women. Reprod Probl. 2001;7 (4):53-61. [Russian].
  7. Danilov RK. Histology manual. Vol II. St. Petersburg: Spets Lit, 2011:513. [Russian].
  8. Savvidis C, Tournis S, Dede AD. Obesity and bone metabolism. Hormones. 2018;17:205-17. CrossRef PubMed
  9. Chooi Yu Chung, Ding C, Magkos F. The epidemiology of obesity. Metabolizm. 2019;92(1):6-10. CrossRef PubMed
  10. Natrus LV, Gayova LV, Byhovets MYu, Osadchuk YuS, Konovalov SE.The value of regulatory effects on lipid metabolism in during complicated diabetes mellitus. Fiziol. Zh. 2020;66(1):25-34. [Ukrainian]. CrossRef
  11. Watt J, Schlezinger JJ. Structurally-diverse, PPARγactivating environmental toxicants induce adipogenesis and suppress osteogenesis in bone marrow mesenchymal stromal cells. Toxicology. 2015;331:66-77. CrossRef PubMed PubMedCentral
  12. Pollock NK. Childhood obesity, bone development, and cardiometabolic risk factors. Mol Cell Endocrinol. 2015;410:52-63. CrossRef PubMed PubMedCentral
  13. Fleet JC, Schoch RD. Molecular mechanisms for regulation of intestinal calcium absorption by vitamin D and other factors. Crit Rev Clin Lab Sci. 2010;47:181-95. CrossRef PubMed PubMedCentral
  14. von Muhlen D, Safii S, Jassal SK, Svartberg J, BarrettConnor E.Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos Int. 2007;18(10):1337-44. CrossRef PubMed
  15. de Paula FJA, Rosen CJ. Bone remodeling and energy metabolism: New perspectives. Bone Res. 2013; 1(1): 72-84. CrossRef PubMed PubMedCentral
  16. Wong SK, Chin K-Y, Suhaimi FH, Ahmad F, Ima-Nirwana S. The relationship between metabolic syndrome and osteoporosis: A review. Nutrients. 2016;8(6):347. CrossRef PubMed PubMedCentral
  17. Shapses SA, Sukumar D. Bone metabolism in obesity and weight loss. Annu Rev Nutr. 2012;32:287-309. CrossRef PubMed PubMedCentral
  18. Bolland MJ, Grey AB, Ames RW, Horne AM, Gamble GD, Reid IR. Fat mass is an important predictor of parathyroid hormone levels in postmenopausal women. Bone. 2006;38:317-21. CrossRef PubMed
  19. Pitroda AP, Harris SS, Dawson-Hughes B. The association of adiposity with parathyroid hormone in healthy older adults. Endocrine. 2009;36:218-23. CrossRef PubMed PubMedCentral
  20. Volkov VP. The morphofunctional state of the parathyroid glands during antipsychotic therapy, depending on age. Universum: medicine and pharmacology: electron. scientific journal, 2015;15(2). Available from https:// cyberleninka.ru ›article› morfofunktsionalnoe. [Rusian].
  21. Drincic AT, Armas LA, Van Diest EE, Heaney RP. Volumetric dilution, rather than sequestration best explains the low vitamin D status of obesity. Obesity (Silver Spring). 2012;20(7):1444-8. CrossRef PubMed
  22. Shapses SA, Pop C, Schneider SH. Vitamin D in Obesity and Weight Loss. In: Weaver CM, Daly RM, BischoffFerrari H, editors. Nutritional Aspects of Osteoporosis. Springer; London. 2016; 9-16. CrossRef
  23. Mateos CG-F, Cayón-Blanco M. Weighthas a weak influence on calcium-phosphorus metabolismin HIVpatients with vitamin D deficiency. 2017:19th Eur. Congress of Endocrinology Endocrine. Abstracts. 2017;49:52. CrossRef
  24. Karra E, Batterham RL. The role of gut hormones in the regulation of body weight and energy homeostasis. Mol Cell Endocrinol. 2010;316:120-8. CrossRef PubMed
  25. Clowes JA, Khosla S, Eastell R. Potential role of pancreatic and enteric hormones in regulating bone turnover. J Bone Miner Res. 2005;20:1497-506. CrossRef PubMed
  26. Cornish J, Callon KE, Bava U, Watson M, Xu X, Lin JM. Preptin, another peptide product of the pancreatic beta-cell, is osteogenic in vitro and in vivo. Am J Physiol Endocrinol Metab. 2007;292:E117-22. CrossRef PubMed
  27. Ishii S, Cauley JA, Crandall CJ, Srikanthan P, Greendale GA, Huang MH, Diabetes and femoral neck strength: findings from the hip strength across the menopausal transition study. J Clin Endocrinol Metab. 2012;97:190-7. CrossRef PubMed PubMedCentral
  28. Srikanthan P, Crandall CJ, Miller-Martinez D, Seeman TE, Greendale GA, Binkley N. Insulin resistance and bone strength: findings from the study of midlife in the United States. J Bone Miner Res, 2014;29:796-803. CrossRef PubMed PubMedCentral
  29. Gutierrez-Rojas I, Lozano D, Nuche-Berenguer B, Moreno P, Acitores A, Ramos-Alvarez I. Amylin exerts osteogenic actions with different efficacy depending on the diabetic status. Mol Cell Endocrinol. 2013;365:309-15. CrossRef PubMed
  30. Greco EA, Lenzi A, Migliaccio S. The obesity of bone. Ther Adv Endocrinol Metab. 2015; 6(6): 273-86. CrossRef PubMed PubMedCentral
  31. Mosca LN, Goldberg TB, da Silva VN, da Silva CC, Kurokawa CS, Bisi Rizzo AC, Corrente JE. Excess body fat negatively affects bone mass in adolescents. Nutrition. 2014;30:847-52. CrossRef PubMed
  32. Wong SK, Chin K-Y, Suhaimi FH, Ahmad F, Ima-Nirwana S. Effects of metabolic syndrome on bone mineral density, histomorphometry and remodelling markers in male rats. PLoS One. 2018;13(2):e0192416. CrossRef PubMed PubMedCentral
  33. Grigoryan OR, Chernova TO, Antsiferov MB. Correction of insulin resistance in postmenopausal women. Reproduct Probl. 2001;7 (4):53-61. [Russian].
  34. Balabolkin MI, Kreminskaya VM. Peculiarities of treatment of insulin independent diabetes mellitus. Ter Arch. 1996;10:5-11. [Russian].
  35. Balabolkin MI. Genetic aspects of diabetes mellitus, ed. Balabolkin MI, Dedov II. Moscow. 2000;2-9. [Russian]. CrossRef
  36. Tokmakova AY. The effectiveness of various methods of conservative therapy in patients with diabetic foot syndrome. Moscow. 1992;22. [Russian].
  37. Klockars A, Levine AS, Olszewski PK. Hypothalamic integration of the endocrine signaling related to food intake. Current Top Behav Neurosci. 2019;43:239-69. CrossRef PubMed
  38. Motyl KJ, Rosen CJ. Understanding leptin-dependent regulation of skeletal homeostasis. Biochimie. 2012; 94:2089-96. CrossRef PubMed PubMedCentral
  39. Mpalaris V, Anagnostis P, Anastasilakis AD, Goulis DG, Doumas A, Iakovou I. Serum leptin, adiponectin and ghrelin concentrations in post-menopausal women: Is there an association with bone mineral density? Maturitas. 2016;88:32-6. CrossRef PubMed
  40. Tang X, Liu G, Kang J, Hou Y, Jiang F, Yuan W, Shi J. Obesity and risk of hip fracture in adults: a metaanalysis of prospective cohort studies. PLoS One. 2013;8(4):e55077. CrossRef PubMed PubMedCentral
  41. Ginzburg MM, Kozupitsa GS. Insulin resistance syndrome. Endocrinol Probl. 1997;43(1):40-3. [Russian]. CrossRef
  42. Thomas T. The complex effects of leptin on bone metabolism through multiple pathways. Current Opin Pharmacol. 2004;4:295-300. CrossRef PubMed
  43. Turner RT, Kalra SP, Wong CP, Philbrick KA, Lindenmaier LB, Boghossian S, et al. Peripheral leptin regulates bone formation. J Bone Miner Res. 2013;28(1):22-34. CrossRef PubMed PubMedCentral
  44. Wang Y, Dellatore P, Douard V, Qin L, Watford M, Ferraris RP. High fat diet enriched with saturated, but not monounsaturated fatty acids adversely affects femur, and both diets increase calcium absorption in older female mice. Nutr Res. 2016;36(7):742-50. CrossRef PubMed PubMedCentral
  45. Rozhinskaya LYa, Marova EI. Osteopenic syndrome in hypothalamic-pituitary diseases. Neuroendocrinology. Clin Essays. Yaroslavl: DIA-press. 1999;423-84. [Russian].
  46. Wong SK, Chin K-Y, Suhaimi FH, Ahmad F, Ima-Nirwana S. The relationship between metabolic syndrome and osteoporosis: A review. Nutrients. 2016; 8(6): 347. CrossRef PubMed PubMedCentral
  47. Khashaeva TX-M, Idrisova MA, Esedova AE, Abusueva ZA, Makhtibekova PA. Bone metabolism, adipokines and obesity in postmenopausal women. Reproduct Probl. 2016;1:74-8. [Russian]. CrossRef
  48. Johansson H, Oden A, Lerner UH, Jutberger H, Lorentzon M, Barrett-Connor E. High serum adiponectin predicts incident fractures in elderly men: Osteoporotic Fractures in Men (MrOS) Sweden. J Bone Miner Res. 2012;27:1390-6. CrossRef PubMed
  49. Berner HS, Lyngstadaas SP, Spahr A, Monjo M, Thommesen L, Drevon CA. Adiponectin and its receptors are expressed in bone-forming cells. Bone. 2004;35:842-9. CrossRef PubMed
  50. Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg Res. 2011;6:30. CrossRef PubMed PubMedCentral
  51. Jurimae J, Kums T, Jurimae T. Adipocytokine and ghrelin levels in relation to bone mineral density in physically active older women: longitudinal associations. Eur J Endocrinol. 2009;160:381-5. CrossRef PubMed
  52. Magni P, Dozio E, Galliera E, Ruscica M, Corsi MM. Molecular aspects of adipokine-bone interactions. Current Mol Med. 2010;10:522-32. CrossRef PubMed
  53. Guri AJ, Bassaganya-Riera J. Systemic effects of white adipose tissue dysregulation and obesity related inflammation. Obesity (Silver Spring). 2011;19:689-700. CrossRef PubMed
  54. Mundy GR. Osteoporosis and inflammation. Nutr Rev. 2007;65:S147-51. CrossRef PubMed
  55. Pfeilschifter J, Koditz R, Pfohl M, Schatz H. Changes in proinflammatory cytokine activity after menopause. Endocrinol Rev. 2002;23:90-119. CrossRef PubMed
  56. Gonnelli S, Caffarelli C, Nuti R. Obesity and fracture risk. Clin Cases Miner Bone Metab. 2014;11:9-14. CrossRef PubMed PubMedCentral
  57. Compston JE, Watts NB, Chapurlat R, Cooper C. Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med. 2011;124: 1043-50. CrossRef PubMed PubMedCentral
  58. Nielson CM, Srikanth P, Orwoll ES. Obesity and fracture in men and women: an epidemiologic perspective. J Bone Miner Res. 2012;27:1-10. CrossRef PubMed
  59. Reid IR. Fat and bone. Arch Biochem Biophys. 2010; 503:20-7. CrossRef PubMed
  60. Tanaka S, Kuroda T, Saito M, Shiraki M. Overweight/ obesity and underweight are both risk factors for osteoporotic fractures at different sites in Japanese postmenopausal women. Osteoporos Int. 2013;24:69-76. CrossRef PubMed
  61. Dimitri P, Bishop N, Walsh JS, Eastell R. Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone. 2012;50:457-66. CrossRef PubMed
  62. Choudhary D, Adhikary S, Gautam J, Maurya P, Ahmad N, Kushwaha P. Detrimental effects of atherogenic and high fat diet on bone and aortic calcification rescued by an isoflavonoid Caviunin β-d-glucopyranoside. Biomed Pharmacother. 2017;92:757-71. CrossRef PubMed
  63. García-Gavilán JF, Bulló M, Canudas S, MartínezGonzález MA, Estruch R, Giardina S. Extra virgin olive oil consumption reduces the risk of osteoporotic fractures in the PREDIMED trial. Clin Nutr pii. 2017; S0261- 5614(17):30006-7.
  64. Minematsu A, Nishii Y, Sakatab S. High-fat/high-sucrose diet results in higher bone mass in aged rats. Bone. 2018;8:18-24. CrossRef PubMed PubMedCentral
  65. Yarrow JF, Toklu HZ, Balaez A, Phillips EG. Fructose consumption does not worsen bone deficits resulting from high-fat feeding in young male rats. Bone. 2016;85:99- CrossRef PubMed PubMedCentral
  66. Yan L, Graef GL, Nielsen FH, Johnson LK, Cao J. Soy protein is beneficial but high-fat diet and voluntary running are detrimental to bone structure in mice. Nutr Res. 2015;35(6):523-31. CrossRef PubMed
  67. Lecka-Czernik B, Stechschulte LA, Czernik PJ, Dowling AR. High bone mass in adult mice with diet-induced obesity results from a combination of initial increase in bone mass followed by attenuation in bone formation; implications for high bone mass and decreased bone quality in obesity. Mol Cell Endocrinol. 2015;410:35-41; CrossRef PubMed
  68. Doucette CR, Horowitz MC, Berry R, MacDougald OA, Anunciado-Koza R, Koza RA, Rosen CJ. A high fat diet increases bone marrow adipose tissue (MAT) but does not alter trabecular or cortical bone mass in C57BL/6J mice. J Cell Physiol. 2015;230(9):2032-7. CrossRef PubMed PubMedCentral
  69. Markovic TP, Natoli SJ. Paradoxical nutritional deficiency in overweight and obesity: the importance of nutrient density. Med J. 2009;190:149-51. CrossRef PubMed
  70. Grethen E, Hill KM, Jones R, Cacucci BM, Gupta CE. Serum leptin, parathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012;97:1655-62. CrossRef PubMed PubMedCentral
  71. Stein EM, Strain G, Sinha N, Ortiz D. Vitamin D insufficiency prior to bariatric surgery: risk factors and a pilot treatment study. Clin Endocrinol. 2009;71:176-83. CrossRef PubMed PubMedCentral
  72. Hsu Y-H, Venners SA, Terwedow HA, Feng Y. Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr. 2006;83:146-54. CrossRef PubMed
  73. Shu L, Beier E, Sheu T, Zhang H. High-fat diet causes bone loss in young mice by promoting osteoclastogenesis through alteration of the bone marrow environment. Calcif Tissue Int. 2015 Apr; 96(4): 313-23. CrossRef PubMed PubMedCentral
  74. Felice JI, Gangoiti MV, Molinuevo MS, McCarthy AD, Cortizo AM. Effects of a metabolic syndrome induced by a fructose-rich diet on bone metabolism in rats. Metabolism. 2014;63(2):296-305. CrossRef PubMed
  75. Felice JI, Schurman L, McCarthy AD, Sedlinsky C, Aguirre JI, Cortizo AM. Effects of fructose-induced metabolic syndrome on rat skeletal cells and tissue, and their responses to metformin treatment. Diabetes Res Clin Pract. 2017;126:202-13. CrossRef PubMed
  76. Li Tian, Xijie Yu Fat, Sugar, and bone health: A complex relationship. Nutrients. 2017;9(5):506. CrossRef PubMed PubMedCentral
  77. Lavet C, Martin A, Linossier MT, Vanden Bossche A Laroche N, Thomas M. Fat and sucrose intake induces obesity-related bone metabolism disturbances: Kinetic and reversibility studies in growing and adult rats. J Bone Min Res. 2016;31(1):98-115. CrossRef PubMed
  78. Minematsu A, Hanaoka T, Takada Y, Okuda S. Femoral bone structure in Otsuka Long-Evans Tokushima Fatty rats. Osteoporos Sarcopen. 2016;2:25-9. CrossRef PubMed PubMedCentral
  79. Minematsu A, Hanaoka T, Takeshita D, Takada Y. Long-term wheel-running can prevent deterioration of bone properties in diabetes mellitus model rats. J. Musculoskelet. Neuronal Interact. 2017;17:433-43.
  80. Dawson-Hughes B, Harris SS, Lichtenstein AH, Dolnikowski G, Palermo NJ, Rasmussen H. Dietary fat increases vitamin D-3 absorption. J Acad Nutr Diet. 2015;115:225-30. CrossRef PubMed
  81. Macri EV, Gonzales Chaves MM, Rodriguez PN. High-fat diets affect energy and bone metabolism in growing rats. Eur J Nutr. 2012;51(4):399-406. CrossRef PubMed

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