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International Journal of Endocrinology
Volume 2018, Article ID 2314769, 8 pages
https://doi.org/10.1155/2018/2314769
Research Article

The Combined Effect of Nonalcoholic Fatty Liver Disease and Metabolic Syndrome on Osteoporosis in Postmenopausal Females in Eastern China

1State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou 310003, China
2Department of Infection and Liver Diseases, Liver Research Center, The First Affiliated Hospital of Wenzhou Medical University, No. 2 Fuxue Lane, Wenzhou 325000, China
3Department of Preventive Medicine, School of Public Health and Management, Wenzhou Medical University, Wenzhou 325000, China

Correspondence should be addressed to Lan-Juan Li; nc.ude.ujz@iljl

Received 8 August 2017; Revised 31 March 2018; Accepted 17 May 2018; Published 29 July 2018

Academic Editor: Thomas J. Fahey

Copyright © 2018 Da-Zhi Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. K. Genant, C. Cooper, G. Poor et al., “Interim report and recommendations of the World Health Organization Task-Force for Osteoporosis,” Osteoporosis International, vol. 10, no. 4, pp. 259–264, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. L.-Q. Yuan, X. Lin, D. Xiong et al., “Epidemiology and management of osteoporosis in the People’s Republic of China: current perspectives,” Clinical Interventions in Aging, vol. 10, pp. 1017–1033, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Li, P. Ou, H. Zhu, D. Yang, and P. Zheng, “Prevalence rate of osteoporosis in the mid-aged and elderly in selected parts of China,” Chinese Medical Journal, vol. 115, no. 5, pp. 773–5, 2002. View at Google Scholar
  4. C. Cooper, The IOF CSA Working Group on Fracture Epidemiology, Z. A. Cole et al., “Secular trends in the incidence of hip and other osteoporotic fractures,” Osteoporosis International, vol. 22, no. 5, pp. 1277–1288, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. US Department of Health and Human Services, Bone Health and Osteoporosis: a Report of the Surgeon General, US Department of Health and Human Services, Office of the Surgeon General, Rockville, MD, USA, 2004.
  6. S. V. Bukata, B. F. DiGiovanni, S. M. Friedman et al., “A guide to improving the care of patients with fragility fractures,” Geriatric Orthopaedic Surgery & Rehabilitation, vol. 2, no. 1, pp. 5–37, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. N. C. Wright, A. C. Looker, K. G. Saag et al., “The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine,” Journal of Bone and Mineral Research, vol. 29, no. 11, pp. 2520–2526, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. B. Abrahamsen, T. van Staa, R. Ariely, M. Olson, and C. Cooper, “Excess mortality following hip fracture: a systematic epidemiological review,” Osteoporosis International, vol. 20, no. 10, pp. 1633–1650, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Marignani and S. Angeletti, “Nonalcoholic fatty liver disease,” The New England Journal of Medicine, vol. 347, no. 10, pp. 768-769, 2002. View at Google Scholar
  10. B. A. Neuschwander-Tetri and S. H. Caldwell, “Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference,” Hepatology, vol. 37, no. 5, pp. 1202–1219, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. S. S. Moon, Y. S. Lee, and S. W. Kim, “Association of nonalcoholic fatty liver disease with low bone mass in postmenopausal women,” Endocrine, vol. 42, no. 2, pp. 423–429, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. K. Jeon, J. G. Lee, S. S. Kim et al., “Association between bone mineral density and metabolic syndrome in pre- and postmenopausal women,” Endocrine Journal, vol. 58, no. 2, pp. 87–93, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Zhou, Q. Zhang, X. Yuan et al., “Association between metabolic syndrome and osteoporosis: a meta-analysis,” Bone, vol. 57, no. 1, pp. 30–35, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Lorentzon and S. R. Cummings, “Osteoporosis: the evolution of a diagnosis,” Journal of Internal Medicine, vol. 277, no. 6, pp. 650–661, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Sambrook and C. Cooper, “Osteoporosis,” The Lancet, vol. 367, no. 9527, pp. 2010–2018, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. J. A. Cauley, “Estrogen and bone health in men and women,” Steroids, vol. 99, no. Part A, pp. 11–15, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Napoli and R. Armamento-Villareal, “Estrogen hydroxylation in osteoporosis,” Advances in Clinical Chemistry, vol. 43, pp. 211–227, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. J. P. Bilezikian, “Osteoporosis in men,” The Journal of Clinical Endocrinology and Metabolism, vol. 84, no. 10, pp. 3431–3434, 1999. View at Publisher · View at Google Scholar
  19. N. B. Watts, R. A. Adler, J. P. Bilezikian et al., “Osteoporosis in men: an Endocrine Society clinical practice guideline,” The Journal of Clinical Endocrinology and Metabolism, vol. 97, no. 6, pp. 1802–1822, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Uchiyama, “Effect of age and anti-osteoporotic drugs on bone strength and structure of the distal radius,” Clinical Calcium, vol. 23, no. 7, pp. 951–958, 2013. View at Google Scholar
  21. J. P. Vandenbroucke, E. von Elm, D. G. Altman et al., “Strengthening the reporting of observational studies in epidemiology (STROBE): explanation and elaboration,” Epidemiology, vol. 18, no. 6, pp. 805–835, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Obika and H. Noguchi, “Diagnosis and evaluation of nonalcoholic fatty liver disease,” Experimental Diabetes Research, vol. 2012, Article ID 145754, 12 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. S. H. Saverymuttu, A. E. Joseph, and J. D. Maxwell, “Ultrasound scanning in the detection of hepatic fibrosis and steatosis,” British Medical Journal (Clinical Research Ed.), vol. 292, no. 6512, pp. 13–15, 1986. View at Publisher · View at Google Scholar · View at Scopus
  24. Cooperative Group for the Study of Metabolic Syndrome in Chinese Diabetes Society, “Recommendations of Chinese Medical Association Diabetes Society for metabolic syndrome,” Chinese Journal of Diabetes, vol. 12, no. 3, pp. 156–161, 2004. View at Google Scholar
  25. T. Andersson, L. Alfredsson, H. Kallberg, S. Zdravkovic, and A. Ahlbom, “Calculating measures of biological interaction,” European Journal of Epidemiology, vol. 20, no. 7, pp. 575–579, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Y. Zou, “On the estimation of additive interaction by use of the four-by-two table and beyond,” American Journal of Epidemiology, vol. 168, no. 2, pp. 212–224, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. M. J. Knol, T. J. VanderWeele, R. H. H. Groenwold, O. H. Klungel, M. M. Rovers, and D. E. Grobbee, “Estimating measures of interaction on an additive scale for preventive exposures,” European Journal of Epidemiology, vol. 26, no. 6, pp. 433–438, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Cui, H. Sheng, X. F. Rui et al., “Low bone mineral density in Chinese adults with nonalcoholic fatty liver disease,” International Journal of Endocrinology, vol. 2013, Article ID 396545, 6 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. M. F. Xia, H. D. Lin, H. M. Yan et al., “The association of liver fat content and serum alanine aminotransferase with bone mineral density in middle-aged and elderly Chinese men and postmenopausal women,” Journal of Translational Medicine, vol. 14, no. 1, p. 11, 2016. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Li, Y. Xu, M. Xu et al., “Association between nonalcoholic fatty liver disease (NAFLD) and osteoporotic fracture in middle-aged and elderly Chinese,” The Journal of Clinical Endocrinology and Metabolism, vol. 97, no. 6, pp. 2033–2038, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. S. H. Lee, J. M. Yun, S. H. Kim et al., “Association between bone mineral density and nonalcoholic fatty liver disease in Korean adults,” Journal of Endocrinological Investigation, vol. 39, no. 11, pp. 1329–1336, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Mofrad, M. J. Contos, M. Haque et al., “Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values,” Hepatology, vol. 37, no. 6, pp. 1286–1292, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Purnak, Y. Beyazit, E. Ozaslan, C. Efe, and M. Hayretci, “The evaluation of bone mineral density in patients with nonalcoholic fatty liver disease,” Wiener Klinische Wochenschrift, vol. 124, no. 15-16, pp. 526–531, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. S. I. McFarlane, “Bone metabolism and the cardiometabolic syndrome: pathophysiologic insights,” Journal of the Cardiometabolic Syndrome, vol. 1, no. 1, pp. 53–57, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. I. I. de Liefde, M. van der Klift, C. E. D. H. de Laet, P. L. A. van Daele, A. Hofman, and H. A. P. Pols, “Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study,” Osteoporosis International, vol. 16, no. 12, pp. 1713–1720, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. L.-H. Cui, M.-H. Shin, S.-S. Kweon et al., “Sex-related differences in the association between waist circumference and bone mineral density in a Korean population,” BMC Musculoskeletal Disorders, vol. 15, no. 1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. K. C. Kim, D. H. Shin, S. Y. Lee, J. A. Im, and D. C. Lee, “Relation between obesity and bone mineral density and vertebral fractures in Korean postmenopausal women,” Yonsei Medical Journal, vol. 51, no. 6, pp. 857–863, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. A. El Maghraoui, A. Rezqi, S. El Mrahi, S. Sadni, I. Ghozlani, and A. Mounach, “Osteoporosis, vertebral fractures and metabolic syndrome in postmenopausal women,” BMC Endocrine Disorders, vol. 14, no. 1, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Kim, S. Park, Y. S. Pak, S. Lee, and E. H. Lee, “Association between metabolic syndrome and bone mineral density in Korea: the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV), 2008,” Journal of Bone and Mineral Metabolism, vol. 31, no. 6, pp. 652–662, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Szulc, A. Varennes, P. D. Delmas, J. Goudable, and R. Chapurlat, “Men with metabolic syndrome have lower bone mineral density but lower fracture risk--the MINOS study,” Journal of Bone and Mineral Research, vol. 25, no. 6, pp. 1446–1454, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Y. Kim, J. W. Choe, H. K. Kim et al., “Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men,” Calcified Tissue International, vol. 86, no. 5, pp. 350–358, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. D. K. Hwang and H. J. Choi, “The relationship between low bone mass and metabolic syndrome in Korean women,” Osteoporosis International, vol. 21, no. 3, pp. 425–431, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Wang, N. Liu, Y. Gao, P. Li, and M. Tian, “Association between metabolic syndrome and osteoporotic fracture in middle-aged and elderly Chinese peoples,” Cell Biochemistry and Biophysics, vol. 70, no. 2, pp. 1297–1303, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Kinjo, S. Setoguchi, and D. H. Solomon, “Bone mineral density in adults with the metabolic syndrome: analysis in a population-based U.S. sample,” The Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 11, pp. 4161–4164, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Lee, “Metabolic syndrome and osteoporosis in relation to muscle mass,” Calcified Tissue International, vol. 97, no. 5, pp. 487–494, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Esposito, P. Chiodini, A. Capuano, A. Colao, and D. Giugliano, “Fracture risk and bone mineral density in metabolic syndrome: a meta-analysis,” The Journal of Clinical Endocrinology and Metabolism, vol. 98, no. 8, pp. 3306–3314, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. L. J. Niebergall, R. L. Jacobs, T. Chaba, and D. E. Vance, “Phosphatidylcholine protects against steatosis in mice but not non-alcoholic steatohepatitis,” Biochimica et Biophysica Acta, vol. 1811, no. 12, pp. 1177–1185, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. R. L. Jacobs, Y. Zhao, D. P. Y. Koonen et al., “Impaired de novo choline synthesis explains why phosphatidylethanolamine N-methyltransferase-deficient mice are protected from diet-induced obesity,” The Journal of Biological Chemistry, vol. 285, no. 29, pp. 22403–22413, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Shen, G. L.-H. Wong, H. L.-Y. Chan et al., “PNPLA3 gene polymorphism accounts for fatty liver in community subjects without metabolic syndrome,” Alimentary Pharmacology & Therapeutics, vol. 39, no. 5, pp. 532–539, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Wainwright and C. Byrne, “Bidirectional relationships and disconnects between NAFLD and features of the metabolic syndrome,” International Journal of Molecular Sciences, vol. 17, no. 3, p. 367, 2016. View at Publisher · View at Google Scholar · View at Scopus
  51. G. I. Russo, S. Cimino, T. Castelli et al., “Benign prostatic hyperplasia, metabolic syndrome and non-alcoholic fatty liver disease: is metaflammation the link?” Prostate, vol. 76, no. 16, pp. 1528–1535, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. H. C. Hong, S. Y. Hwang, J. Y. Ryu et al., “The synergistic impact of nonalcoholic fatty liver disease and metabolic syndrome on subclinical atherosclerosis,” Clinical Endocrinology, vol. 84, no. 2, pp. 203–209, 2016. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Yilmaz, “Review article: non-alcoholic fatty liver disease and osteoporosis--clinical and molecular crosstalk,” Alimentary Pharmacology & Therapeutics, vol. 36, no. 4, pp. 345–352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Targher, A. Lonardo, and M. Rossini, “Nonalcoholic fatty liver disease and decreased bone mineral density: is there a link?” Journal of Endocrinological Investigation, vol. 38, no. 8, pp. 817–825, 2015. View at Publisher · View at Google Scholar · View at Scopus
  55. C. A. Peterson and M. E. Heffernan, “Serum tumor necrosis factor-alpha concentrations are negatively correlated with serum 25(OH)D concentrations in healthy women,” Journal of Inflammation, vol. 5, no. 1, p. 10, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. S. Nanes, “Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology,” Gene, vol. 321, pp. 1–15, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. H. L. Lee, T. Yi, K. M. Woo, H. M. Ryoo, G. S. Kim, and J. H. Baek, “Msx2 mediates the inhibitory action of TNF-α on osteoblast differentiation,” Experimental & Molecular Medicine, vol. 42, no. 6, pp. 437–445, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Wong, K.-Y. Chin, F. Suhaimi, F. Ahmad, and S. Ima-Nirwana, “The relationship between metabolic syndrome and osteoporosis: a review,” Nutrients, vol. 8, no. 6, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. A. E. A. Joseph, S. H. Saverymuttu, S. Al-Sam, M. G. Cook, and J. D. Maxwell, “Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease,” Clinical Radiology, vol. 43, no. 1, pp. 26–31, 1991. View at Publisher · View at Google Scholar · View at Scopus