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Effects of metabolic syndrome on jawbones and bone metabolic markers in sucrose-fed rats

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Abstract

The aim of this study was to investigate the effects of metabolic syndrome (MetS) on bone mineral density (BMD) and microstructure of jawbones, and circulating bone metabolic markers. MetS was induced in male Wistar rats by a 16-week high-sucrose drinking water diet. Mandibles were analyzed for BMD and microstructure by standard radiographs and X-ray diffraction. BMD of three different regions of mandible in MetS group was significantly lower compared to control group. The diffraction intensity of mandibular bone in MetS group was significantly decreased (8.2%) compared to control group; however, crystallite radiuses of mandibular bone samples in both groups were not significantly different. In MetS group, serum bone-specific tartrate-resistant acid phosphatase-5b (TRACP-5b) activity was significantly increased (47%), whereas bone-specific alkaline phosphatase (BALP) activity was significantly decreased (44%) compared to control group. The serum magnesium level in MetS rats (1.82 ± 0.27 mg dL−1) was lower than that of controls (2.11 ± 0.16 mg dL−1). Rats with MetS had significantly higher serum calcium level (9.70 ± 0.41 mg dL−1) than the controls (9.21 ± 0.50 mg dL−1). Overall data suggested that MetS is associated with a significant decrease in BMD and slight deterioration in microcrystallite structure of the jawbones. The changes in TRACP-5b and BALP activities and serum Ca2+ and Mg2+ concentrations also support these findings at a biochemical level.

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References

  1. Kaur J. A comprehensive review on metabolic syndrome. Cardiol Res Pract. 2014;2014:943162. https://doi.org/10.1155/2014/943162.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Goldenberg R, Punthakee Z. Definition, classification and diagnosis of diabetes, prediabetes and metabolic syndrome. Can J Diabetes. 2013;37(Suppl 1):8–11. https://doi.org/10.1016/j.jcjd.2013.01.011.

    Article  Google Scholar 

  3. O’Neill S, O’Driscoll L. Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies. Obes Rev. 2015;16(1):1–12. https://doi.org/10.1111/obr.12229.

    Article  PubMed  Google Scholar 

  4. Yamaoka K, Tango T. Effects of lifestyle modification on metabolic syndrome: a systematic review and meta-analysis. BMC Med. 2012;10:138. https://doi.org/10.1186/1741-7015-10-138.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Yaturu S, Humphrey S, Landry C, Jain SK. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2009;15(1):CR5–9.

    PubMed  Google Scholar 

  6. Kim HY, Choe JW, Kim HK, Bae SJ, Kim BJ, Lee SH, Koh JM, Han KO, Park HM, Kim GS. Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men. Calcif Tissue Int. 2010;86(5):350–8. https://doi.org/10.1007/s00223-010-9347-2.

    Article  PubMed  Google Scholar 

  7. Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R. Men with metabolic syndrome have lower bone mineral density but lower fracture risk—the MINOS study. J Bone Miner Res. 2010;25(6):1446–54. https://doi.org/10.1002/jbmr.13.

    Article  PubMed  Google Scholar 

  8. DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14(3):173–94.

    Article  Google Scholar 

  9. von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor 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. https://doi.org/10.1007/s00198-007-0385-1.

    Article  Google Scholar 

  10. Yamaguchi T, Kanazawa I, Yamamoto M, Kurioka S, Yamauchi M, Yano S, Sugimoto T. Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone. 2009;45(2):174–9. https://doi.org/10.1016/j.bone.2009.05.003.

    Article  PubMed  Google Scholar 

  11. Dutta M, Pakhetra R, Garg M. Evaluation of bone mineral density in type 2 diabetes mellitus patients before and after treatment. Med J Armed Forces India. 2012;68(1):48–52. https://doi.org/10.1016/S0377-1237(11)60120-2.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Tsanzi E, Light HR, Tou JC. The effect of feeding different sugar-sweetened beverages to growing female Sprague–Dawley rats on bone mass and strength. Bone. 2008;42(5):960–8. https://doi.org/10.1016/j.bone.2008.01.020.

    Article  PubMed  Google Scholar 

  13. Hernandez JL, Olmos JM, Pariente E, Martinez J, Valero C, Garcia-Velasco P, Nan D, Llorca J, Gonzalez-Macias J. Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause. 2010;17(5):955–61. https://doi.org/10.1097/gme.0b013e3181e39a15.

    Article  PubMed  Google Scholar 

  14. Sun M, Cao M, Fu Q, Zhu Z, Meng C, Mao J, Shi Y, Duan Y, Tang W, Huang X, He W, Yang T. Association of calcaneal quantitative ultrasound parameters with metabolic syndrome in middle-aged and elderly Chinese: a large population-based cross-sectional study. BMC Endocr Disord. 2014;14:14. https://doi.org/10.1186/1472-6823-14-14.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lee K. Metabolic syndrome and osteoporosis in relation to muscle mass. Calcif Tissue Int. 2015;97(5):487–94. https://doi.org/10.1007/s00223-015-0033-2.

    Article  PubMed  Google Scholar 

  16. Muka T, Trajanoska K, Kiefte-de Jong JC, Oei L, Uitterlinden AG, Hofman A, Dehghan A, Zillikens MC, Franco OH, Rivadeneira F. The association between metabolic syndrome, bone mineral density, hip bone geometry and fracture risk: the Rotterdam study. PLoS One. 2015;10(6):e0129116. https://doi.org/10.1371/journal.pone.0129116.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Smith BJ, Lerner MR, Bu SY, Lucas EA, Hanas JS, Lightfoot SA, Postier RG, Bronze MS, Brackett DJ. Systemic bone loss and induction of coronary vessel disease in a rat model of chronic inflammation. Bone. 2006;38(3):378–86. https://doi.org/10.1016/j.bone.2005.09.008.

    Article  PubMed  Google Scholar 

  18. Campos RM, de Piano A, da Silva PL, Carnier J, Sanches PL, Corgosinho FC, Masquio DC, Lazaretti-Castro M, Oyama LM, Nascimento CM, Tock L, de Mello MT, Tufik S, Damaso AR. The role of pro/anti-inflammatory adipokines on bone metabolism in NAFLD obese adolescents: effects of long-term interdisciplinary therapy. Endocrine. 2012;42(1):146–56. https://doi.org/10.1007/s12020-012-9613-3.

    Article  PubMed  Google Scholar 

  19. Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Kurioka S, Yano S, Sugimoto T. Serum osteocalcin level is associated with glucose metabolism and atherosclerosis parameters in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2009;94(1):45–9. https://doi.org/10.1210/jc.2008-1455.

    Article  PubMed  Google Scholar 

  20. Ohnishi T, Bandow K, Kakimoto K, Machigashira M, Matsuyama T, Matsuguchi T. Oxidative stress causes alveolar bone loss in metabolic syndrome model mice with type 2 diabetes. J Periodontal Res. 2009;44(1):43–51. https://doi.org/10.1111/j.1600-0765.2007.01060.x.

    Article  PubMed  Google Scholar 

  21. 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. https://doi.org/10.1016/j.diabres.2017.02.011.

    Article  PubMed  Google Scholar 

  22. 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. https://doi.org/10.1016/j.metabol.2013.11.002.

    Article  PubMed  Google Scholar 

  23. Fujita Y, Maki K. High-fat diet-induced obesity triggers alveolar bone loss and spontaneous periodontal disease in growing mice. BMC Obes. 2015;3:1. https://doi.org/10.1186/s40608-016-0082-8.

    Article  PubMed  Google Scholar 

  24. Bagi CM, Edwards K, Berryman E. Metabolic syndrome and bone: pharmacologically induced diabetes has deleterious effect on bone in growing obese rats. Calcif Tissue Int. 2018;102(6):683–94. https://doi.org/10.1007/s00223-017-0367-z.

    Article  PubMed  Google Scholar 

  25. Montalvany-Antonucci CC, Zicker MC, Macari S, Pereira TSF, Diniz IMA, Andrade I Jr, Ferreira AVM, Silva TA. High-refined carbohydrate diet promotes detrimental effects on alveolar bone and femur microarchitecture. Arch Oral Biol. 2018;86:101–7. https://doi.org/10.1016/j.archoralbio.2017.11.013.

    Article  PubMed  Google Scholar 

  26. Zhou WH, Zhang JK, Lin KL, Chen FS. Comparison between mandibular and femur derived bone marrow stromal cells: osteogenic and angiogenic potentials in vitro and bone repairing ability in vivo. Rsc Adv. 2017;7(89):56220–8. https://doi.org/10.1039/c7ra07139f.

    Article  Google Scholar 

  27. de Souza Faloni AP, Schoenmaker T, Azari A, Katchburian E, Cerri PS, de Vries TJ, Everts V. Jaw and long bone marrows have a different osteoclastogenic potential. Calcif Tissue Int. 2011;88(1):63–74. https://doi.org/10.1007/s00223-010-9418-4.

    Article  PubMed  Google Scholar 

  28. Mavropoulos A, Rizzoli R, Ammann P. Different responsiveness of alveolar and tibial bone to bone loss stimuli. J Bone Miner Res. 2007;22(3):403–10. https://doi.org/10.1359/jbmr.061208.

    Article  Google Scholar 

  29. Tanaka M, Ejiri S, Kohno S, Ozawa H. Region-specific bone mass changes in rat mandibular condyle following ovariectomy. J Dent Res. 2000;79(11):1907–13. https://doi.org/10.1177/00220345000790111601.

    Article  PubMed  Google Scholar 

  30. Rosalki SB, Foo AY. Two new methods for separating and quantifying bone and liver alkaline phosphatase isoenzymes in plasma. Clin Chem. 1984;30(7):1182–6.

    PubMed  Google Scholar 

  31. Mizoguchi I, Toriya N, Nakao Y. Growth of the mandible and biological characteristics of the mandibular condylar cartilage. Jpn Dent. Sci. Rev. 2013;49(4):139–50. https://doi.org/10.1016/j.jdsr.2013.07.004.

    Article  Google Scholar 

  32. Greco EA, Fornari R, Rossi F, Santiemma V, Prossomariti G, Annoscia C, Aversa A, Brama M, Marini M, Donini LM, Spera G, Lenzi A, Lubrano C, Migliaccio S. Is obesity protective for osteoporosis? Evaluation of bone mineral density in individuals with high body mass index. Int J Clin Pract. 2010;64(6):817–20. https://doi.org/10.1111/j.1742-1241.2009.02301.x.

    Article  PubMed  Google Scholar 

  33. Cakur B, Dagistan S, Sahin A, Harorli A, Yilmaz A. Reliability of mandibular cortical index and mandibular bone mineral density in the detection of osteoporotic women. Dentomaxillofac Radiol. 2009;38(5):255–61. https://doi.org/10.1259/dmfr/22559806.

    Article  PubMed  Google Scholar 

  34. Smith EE, Ferguson VL, Simske SJ, Gayles EC, Pagliassotti MJ. Effects of high fat or high sucrose diets on rat femora mechanical and compositional properties. Biomed Sci Instrum. 2000;36:385–90.

    PubMed  Google Scholar 

  35. Tjaderhane L, Larmas M. A high sucrose diet decreases the mechanical strength of bones in growing rats. J Nutr. 1998;128(10):1807–10.

    Article  PubMed  Google Scholar 

  36. Softic S, Cohen DE, Kahn CR. Role of dietary fructose and hepatic de novo lipogenesis in fatty liver disease. Dig Dis Sci. 2016;61(5):1282–93. https://doi.org/10.1007/s10620-016-4054-0.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ferder L, Inserra F, Martinez-Maldonado M. Inflammation and the metabolic syndrome: role of angiotensin II and oxidative stress. Curr Hypertens Rep. 2006;8(3):191–8.

    Article  PubMed  Google Scholar 

  38. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism. 2008;57(8):1071–7. https://doi.org/10.1016/j.metabol.2008.03.010.

    Article  PubMed  Google Scholar 

  39. Tukel HC, Alptekin O, Turan B, Delilbasi E. Effects of metabolic syndrome on masseter muscle of male Wistar rats. Eur J Oral Sci. 2015;123(6):432–8. https://doi.org/10.1111/eos.12226.

    Article  PubMed  Google Scholar 

  40. Li Y, Lu Z, Zhang X, Yu H, Kirkwood KL, Lopes-Virella MF, Huang Y. Metabolic syndrome exacerbates inflammation and bone loss in periodontitis. J Dent Res. 2015;94(2):362–70. https://doi.org/10.1177/0022034514561658.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Kaye EK, Chen N, Cabral HJ, Vokonas P, Garcia RI. Metabolic syndrome and periodontal disease progression in men. J Dent Res. 2016;95(7):822–8. https://doi.org/10.1177/0022034516641053.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Halleen JM, Tiitinen SL, Ylipahkala H, Fagerlund KM, Vaananen HK. Tartrate-resistant acid phosphatase 5b (TRACP 5b) as a marker of bone resorption. Clin Lab. 2006;52(9–10):499–509.

    PubMed  Google Scholar 

  43. Cheung CL, Tan KC, Lam KS, Cheung BM. The relationship between glucose metabolism, metabolic syndrome, and bone-specific alkaline phosphatase: a structural equation modeling approach. J Clin Endocrinol Metab. 2013;98(9):3856–63. https://doi.org/10.1210/jc.2013-2024.

    Article  PubMed  Google Scholar 

  44. Kim MK, Kim G, Jang EH, Kwon HS, Baek KH, Oh KW, Lee JH, Yoon KH, Lee WC, Lee KW, Son HY, Kang MI. Altered calcium homeostasis is correlated with the presence of metabolic syndrome and diabetes in middle-aged and elderly Korean subjects: the Chungju Metabolic Disease Cohort study (CMC study). Atherosclerosis. 2010;212(2):674–81. https://doi.org/10.1016/j.atherosclerosis.2010.07.005.

    Article  PubMed  Google Scholar 

  45. Saltevo J, Niskanen L, Kautiainen H, Teittinen J, Oksa H, Korpi-Hyovalti E, Sundvall J, Mannisto S, Peltonen M, Mantyselka P, Vanhala M. Serum calcium level is associated with metabolic syndrome in the general population: FIN-D2D study. Eur J Endocrinol. 2011;165(3):429–34. https://doi.org/10.1530/EJE-11-0066.

    Article  PubMed  Google Scholar 

  46. Guerrero-Romero F, Rodriguez-Moran M. Hypomagnesemia, oxidative stress, inflammation, and metabolic syndrome. Diabetes Metab Res Rev. 2006;22(6):471–6. https://doi.org/10.1002/dmrr.644.

    Article  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. Esma N. Okatan for her help with the animal handling and we would like to thank Begum Selen Uzun for her help with statistical analysis. The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

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  1. Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Çukurova University, 01330, Adana, Turkey

    Hüseyin Can Tükel

  2. Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Gazi University, Ankara, Turkey

    Ertan Delilbaşı

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Tükel, H.C., Delilbaşı, E. Effects of metabolic syndrome on jawbones and bone metabolic markers in sucrose-fed rats. Odontology 107, 457–464 (2019). https://doi.org/10.1007/s10266-019-00422-w

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