Smoking and other determinants of bone turnover
Autoři:
Rolf Jorde aff001; Astrid Kamilla Stunes aff003; Julia Kubiak aff001; Guri Grimnes aff001; Per Medbøe Thorsby aff005; Unni Syversen aff003
Působiště autorů:
Tromsø Endocrine Research Group, Department of Clinical Medicine, UiT, The Arctic University of Norway, Tromsø, Norway
aff001; Division of Internal Medicine, University Hospital of North Norway, Tromsø, Norway
aff002; Department of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway
aff003; Clinic of Medicine, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway
aff004; Hormone Laboratory, Department of Medical Biochemistry, Oslo University Hospital, Aker Hospital, Oslo, Norway
aff005; Department of Endocrinology, Clinic of Medicine, St. Olav’s Hospital, Trondheim University Hospital, Trondheim, Norway
aff006
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225539
Souhrn
The balance between bone resorption and formation may be assessed by measurement of bone turnover markers (BTMs), like carboxyl-terminal cross-linked telopeptide of type 1 collagen (CTX-1) and procollagen type 1 amino-terminal propeptide (P1NP). Smoking has been shown to influence bone turnover and to reduce bone mass density (BMD), the exact mechanism for this is, however, not settled. In this post-hoc study including 406 subjects (mean age 51.9 years), we aimed to study the impact of smoking on bone turnover. Moreover, we wanted to assess the inter-correlation between substances regulating bone metabolism and BTMs, as well as tracking over time. BMD measurements and serum analyses of CTX-1, P1NP, osteoprotegerin (OPG), receptor activator of nuclear factor ĸB ligand (RANKL), Dickkopf-1 (DKK1), sclerostin, tumor necrosis factor-α (TNF-α), and leptin were performed. Repeated serum measurements were made in 195 subjects after four months. Adjustments were made for sex, age, body mass index (BMI), smoking status, insulin resistance, serum calcium, parathyroid hormone, 25-hydroxyvitamin D and creatinine. Smokers had higher levels of DKK1 and OPG, and lower levels of RANKL, as reflected in lower BTMs and BMD compared to non-smokers. There were strong and predominantly positive inter-correlations between BTMs and the other substances, and there was a high degree of tracking with Spearman’s rho from 0.72 to 0.92 (P < 0.001) between measurements four months apart. In conclusion, smokers exhibited higher levels of DKK1 and OPG and a lower bone turnover than did non-smokers. The strong inter-correlations between the serum parameters illustrate the coupling between bone resorption and formation and crosstalk between cells.
Klíčová slova:
leptin – Hip – Smoking habits – Creatinine – Bone development – Bone resorption
Zdroje
1. Tanaka Y, Nakayamada S, Okada Y. Osteoblasts and osteoclasts in bone remodeling and inflammation. Curr Drug Targets Inflamm Allergy. 2005; 4:325–8. doi: 10.2174/1568010054022015 16101541
2. Ikeda K, Takeshita S. Factors and mechanisms involved in the coupling from bone resorption to formation: how osteoclasts talk to osteoblasts. J Bone Metab. 2014; A21(3):163–7.
3. Eastell R, Pigott T, Gossiel F, Naylor KE, Walsh JS, Peel NFA. DIAGNOSIS OF ENDOCRINE DISEASE: Bone turnover markers: are they clinically useful? Eur J Endocrinol. 2018; 178:R19–R31. doi: 10.1530/EJE-17-0585 29046326
4. Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A, et al. Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int. 2011; 22:391–420. doi: 10.1007/s00198-010-1501-1 21184054
5. Martin TJ, Sims NA. RANKL/OPG; Critical role in bone physiology. Rev Endocr Metab Disord. 2015; 16:131–9. doi: 10.1007/s11154-014-9308-6 25557611
6. Zhao B. TNF and Bone Remodeling. Curr Osteoporos Rep. 2017; 15:126–34. doi: 10.1007/s11914-017-0358-z 28477234
7. Delgado-Calle J, Sato AY, Bellido T. Role and mechanism of action of sclerostin in bone. Bone. 2017; 96:29–37. doi: 10.1016/j.bone.2016.10.007 27742498
8. Reseland JE, Syversen U, Bakke I, Qvigstad G, Eide LG, Hjertner O, et al. Leptin is expressed in and secreted from primary cultures of human osteoblasts and promotes bone mineralization. J Bone Miner Res. 2001; 16:1426–33. doi: 10.1359/jbmr.2001.16.8.1426 11499865
9. Goltzman D. Functions of vitamin D in bone. Histochem Cell Biol. 2018; 149:305–12. doi: 10.1007/s00418-018-1648-y 29435763
10. Yoon V, Maalouf NM, Sakhaee K. The effects of smoking on bone metabolism. Osteoporos Int. 2012; 23:2081–92. doi: 10.1007/s00198-012-1940-y 22349964
11. Viljakainen H, Ivaska KK, Paldánius P, Lipsanen-Nyman M, Saukkonen T, Pietiläinen KH, et al. Suppressed bone turnover in obesity: a link to energy metabolism? A case-control study. J Clin Endocrinol Metab. 2014; 99:2155–63. doi: 10.1210/jc.2013-3097 24606073
12. Al-Bashaireh AM, Haddad LG, Weaver M, Chengguo X, Kelly DL, Yoon S. The Effect of Tobacco Smoking on Bone Mass: An overview of Pathophysiological Mechanisms. J Osteoporos. 2018; 2018:1206235. doi: 10.1155/2018/1206235 30631414
13. Kubiak J, Kamycheva E, Jorde R. Vitamin D supplementation does not improve CVD risk factors in vitamin D-insufficient subjects. Endocr Connect. 2018; 7:840–9. doi: 10.1530/EC-18-0144 29764903
14. Jorde R, Stunes AK, Kubiak J, Joakimsen R, Grimnes G, Thorsby PM, et al. Effects of vitamin D supplementation on bone turnover markers and other bone-related substances in subjects with vitamin D deficiency. Bone. 2019; 124:7–13. doi: 10.1016/j.bone.2019.04.002 30959189
15. Jacobsen BK, Eggen AE, Mathiesen EB, Wilsgaard T, Njølstad I. Cohort profile: the Tromso Study. Int J Epidemiol. 2012; 41:961–7. doi: 10.1093/ije/dyr049 21422063
16. Register TC, Hruska KA, Divers J, Bowden DW, Palmer ND, Carr JJ, et al. Sclerostin is positively associated with bone mineral density in men and women and negatively associated with carotid calcified atherosclerotic plaque in men from the African American-Diabetes Heart Study. J Clin Endocrinol Metab. 2014; 99:315–21. doi: 10.1210/jc.2013-3168 24178795
17. Reseland JE, Mundal HH, Hollung K, Haugen F, Zahid N, Anderssen SA, et al. Cigarette smoking may reduce plasma leptin concentration via catecholamines. Prostaglandins Leukot Essent Fatty Acids. 2005; 73:43–9. doi: 10.1016/j.plefa.2005.04.006 15964536
18. Secchiero P, Corallini F, Pandolfi A, Consoli A, Candido R, Fabris B, et al. An increased osteoprotegerin serum release characterizes the early onset of diabetes mellitus and may contribute to endothelial cell dysfunction. Am J Pathol. 2006; 169:2236–44. doi: 10.2353/ajpath.2006.060398 17148684
19. Fujiyoshi A, Polgreen LE, Gross MD, Reis JP, Sidney S, Jacobs DR Jr. Smoking habits and parathyroid hormone concentrations in young adults: The CARDIA study. Bone Rep. 2016; 5:104–9. doi: 10.1016/j.bonr.2016.04.003 27795978
20. Khan TS, Fraser LA. Type 1 diabetes and osteoporosis: from molecular pathways to bone phenotype. J Osteoporos. 2015; 2015:174186. doi: 10.1155/2015/174186 25874154
21. Compston J. Type 2 diabetes mellitus and bone. J Intern Med. 2018; 283:140–53. doi: 10.1111/joim.12725 29265670
22. Kanis JA, Johnell O, Oden A, Johansson H, De Laet C, Eisman JA, et al. Smoking and fracture risk: a meta-analysis. Osteoporos Int. 2005; 16:155–62. doi: 10.1007/s00198-004-1640-3 15175845
23. Farr JN, Drake MT, Amin S, Melton LJ 3rd, McCready LK, Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014; 29:787–95. doi: 10.1002/jbmr.2106 24123088
24. Steptoe A, Ussher M. Smoking, cortisol and nicotine. Int J Psychophysiol. 2006; 59:228–35. doi: 10.1016/j.ijpsycho.2005.10.011 16337291
25. Komori T. Glucocorticoid Signaling and Bone Biology. Horm Metab Res. 2016; 48:755–63. doi: 10.1055/s-0042-110571 27871116
26. Tanaka H, Tanabe N, Kawato T, Nakai K, Kariya T, Matsumoto S, et al. Nicotine affects bone resorption and suppresses the expression of cathepsin K, MMP-9 and vacuolar-type H(+)-ATPase d2 and actin organization in osteoclasts. PLoS One. 2013; 8:e59402. doi: 10.1371/journal.pone.0059402 23555029
27. Yun C, Weiner JA, Chun DS, Yun J, Cook RW, Schallmo MS, et al. Mechanistic insight intothe effects of Aryl Hydrocarbon Receptor activation on osteogenic differentiation. Bone Rep. 2017; 6:51–9. doi: 10.1016/j.bonr.2017.02.003 28377982
28. Voronov I, Li K, Tenenbaum HC, Manolson MF. Benzo[a]pyrene inhibits osteoclastogenesis by affecting RANKL-induced activation of NF-kappaB. Biochem Pharmacol. 2008; 75:2034–44. doi: 10.1016/j.bcp.2008.02.025 18396263
29. Caruso RV, O'Connor RJ, Stephens WE, Cummings KM, Fong GT. Toxic metal concentrations in cigarettes obtained from U.S. smokers in 2009: results from the International Tobacco Control (ITC) United States survey cohort. Int J Environ Res Public Health. 2013; 11:202–17. doi: 10.3390/ijerph110100202 24452255
30. Rodríguez J, Mandalunis PM. A Review of Metal Exposure and Its Effects on Bone Health. J Toxicol. 2018; 2018:4854152. doi: 10.1155/2018/4854152 30675155
31. Ibrahim KS, Beshir S, Shahy EM, Shaheen W. Effect of Occupational Cadmium Exposure on Parathyroid Gland. Open Access Maced J Med Sci. 2016; 4:302–6. doi: 10.3889/oamjms.2016.042 27335606
32. Kotlinska-Hasiec E, Makara-Studzinska M, Czajkowski M, Rzecki Z, Olszewski K, Stadnik A, et al. Plasma magnesium concentrations in patients undergoing coronary artery bypass grafting. Ann Agric Environ Med. 2017; 24:181–4. doi: 10.5604/12321966.1232767 28664690
33. Jorde R, Saleh F, Figenschau Y, Kamycheva E, Haug E, Sundsfjord J. Serum parathyroid hormone (PTH) levels in smokers and non-smokers. The fifth Tromsø study. Eur J Endocrinol. 2005; 152:39–45. doi: 10.1530/eje.1.01816 15762185
34. Degens H, Gayan-Ramirez G, van Hees HW. Smoking-induced skeletal muscle dysfunction: from evidence to mechanisms. Am J Respir Crit Care Med. 2015; 191:620–5. doi: 10.1164/rccm.201410-1830PP 25581779
35. Halimi JM, Giraudeau B, Vol S, Cacès E, Nivet H, Lebranchu Y, et al. Effects of current smoking and smoking discontinuation on renal function and proteinuria in the general population. Kidney Int. 2000; 58:1285–92. doi: 10.1046/j.1523-1755.2000.00284.x 10972692
36. Holloway-Kew KL, De Abreu LLF, Kotowicz MA, Sajjad MA, Pasco JA. Bone Turnover Markers in Men and Women with Impaired Fasting Glucose and Diabetes. Calcif Tissue Int. 2019; 104:599–604. doi: 10.1007/s00223-019-00527-y 30680432
37. Fernandes TAP, Gonçalves LML, Brito JAA. Relationships between Bone Turnover and Energy Metabolism. J Diabetes Res. 2017; 2017:9021314. doi: 10.1155/2017/9021314 28695134
38. Duan P, Yang M, Wei M, Liu J, Tu P. Serum Osteoprotegerin Is a Potential Biomarker of Insulin Resistance in Chinese Postmenopausal Women with Prediabetes and Type 2 Diabetes. Int J Endocrinol. 2017; 2017:8724869. doi: 10.1155/2017/8724869 28255300
39. Kiechl S, Wittmann J, Giaccari A, Knoflach M, Willeit P, Bozec A, et al. Blockade of receptor activator of nuclear factor-κB (RANKL) signaling improves hepatic insulin resistance and prevents development of diabetes mellitus. Nat Med. 2013; 19:358–63. doi: 10.1038/nm.3084 23396210
40. Zuo H, Shi Z, Yuan B, Dai Y, Wu G, Hussain A. Association between serum leptin concentrations and insulin resistance: a population-based study from China. PLoS One. 2013; 8:e54615. doi: 10.1371/journal.pone.0054615 23349940
41. Miyazaki Y, Pipek R, Mandarino LJ, DeFronzo RA. Tumor necrosis factor alpha and insulin resistance in obese type 2 diabetic patients. Int J Obes Relat Metab Disord. 2003; 27:88–94. doi: 10.1038/sj.ijo.0802187 12532159
42. Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, et al. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell. 2010; 142:296–308. doi: 10.1016/j.cell.2010.06.003 20655470
43. Shao J, Wang Z, Yang T, Ying H, Zhang Y, Liu S. Bone Regulates Glucose Metabolism as an Endocrine Organ through Osteocalcin. Int J Endocrinol. 2015; 2015: 967673. doi: 10.1155/2015/967673 25873961
44. Amrein K, Amrein S, Drexler C, Dimai HP, Dobnig H, Pfeifer K, et al. Sclerostin and its association with physical activity, age, gender, body composition, and bone mineral content in healthy adults. J Clin Endocrinol Metab. 2012; 97:148–54. doi: 10.1210/jc.2011-2152 21994959
45. Hipmair G, Böhler N, Maschek W, Soriguer F, Rojo-Martínez G, Schimetta W, et al. Serum leptin is correlated to high turnover in osteoporosis. Neuro Endocrinol Lett. 2010; 31:155–60. 20150868
46. Ganji V, Kafai MR, McCarthy E. Serum leptin concentrations are not related to dietary patterns but are related to sex, age, body mass index, serum triacylglycerol, serum insulin, and plasma glucose in the US population. Nutr Metab. 2009; 6:3.
47. Baumgartner RN, Ross RR, Waters DL, Brooks WM, Morley JE, Montoya GD, et al. Serum leptin in elderly people: associations with sex hormones, insulin, and adipose tissue volumes. Obes Res. 1999; 7:141–9. doi: 10.1002/j.1550-8528.1999.tb00695.x 10102250
48. Altinova AE, Toruner F, Akturk M, Bukan N, Yetkin I, Cakir N, et al. Relationship between serum osteoprotegerin, glycemic control, renal function and markers of atherosclerosis in type 2 diabetes. Scand J Clin Lab Invest. 2011; 71:340–3. doi: 10.3109/00365513.2011.570868 21486111
49. Shinkov AD, Borissova AM, Kovatcheva RD, Atanassova IB, Vlahov JD, Dakovska LN. Age and menopausal status affect osteoprotegerin and osteocalcin levels in women differently, irrespective of thyroid function. Clin Med Insights Endocrinol Diabetes. 2014; 7:19–24. doi: 10.4137/CMED.S15466 25125991
50. Redmond J, Fulford AJ, Jarjou L, Zhou B, Prentice A, Schoenmakers I. Diurnal Rhythms of Bone Turnover Markers in Three Ethnic Groups. J Clin Endocrinol Metab. 2016; 101:3222–30. doi: 10.1210/jc.2016-1183 27294326
51. Bjarnason NH, Henriksen EE, Alexandersen P, Christgau S, Henriksen DB, Christiansen C. Mechanism of circadian variation in bone resorption. Bone. 2002; 30:307–13. doi: 10.1016/s8756-3282(01)00662-7 11792602
52. Jorde R, Sneve M, Hutchinson M, Emaus N, Figenschau Y, Grimnes G. Tracking of serum 25-hydroxyvitamin D levels during 14 years in a population-based study and during 12 months in an intervention study. Am J Epidemiol. 2010; 171:903–8. doi: 10.1093/aje/kwq005 20219763
53. Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, Hangartner TN, et al. Tracking of bone mass and density during childhood and adolescence. J Clin Endocrinol Metab. 2010; 95:1690–8. doi: 10.1210/jc.2009-2319 20194709
54. Gruszfeld D, Kułaga Z, Wierzbicka A, Rzehak P, Grote V, Martin F, et al. Leptin and Adiponectin Serum Levels from Infancy to School Age: Factors Influencing Tracking. Child Obes. 2016; 12:179–87. doi: 10.1089/chi.2015.0245 27027910
55. Li LJ, Rifas-Shiman SL, Aris IM, Mantzoros C, Hivert MF, Oken E. Leptin trajectories from birth to mid-childhood and cardio-metabolic health in early adolescence. Metabolism. 2019; 91:30–8. doi: 10.1016/j.metabol.2018.11.003 30412696
56. Chang MC, Chen YJ, Lian YC, Chang BE, Huang CC, Huang WL, et al. Butyrate Stimulates Histone H3 Acetylation, 8-Isoprostane Production, RANKL Expression, and Regulated Osteoprotegerin Expression/Secretion in MG-63 Osteoblastic Cells. Int J Mol Sci. 2018; 19:4071.
57. Mohamed HG, Idris SB, Mustafa M, Ahmed MF, Åstrøm AN, Mustafa K, et al. Influence of Type 2 Diabetes on Prevalence of Key Periodontal Pathogens, Salivary Matrix Metalloproteinases, and Bone Remodeling Markers in Sudanese Adults with and without Chronic Periodontitis. Int J Dent. 2016; 2016:6296854. doi: 10.1155/2016/6296854 26989414
58. Bauer S, Hofbauer LC, Rauner M, Strzelczyk A, Kellinghaus C, Hallmeyer-Elgner S, et al. Early detection of bone metabolism changes under different antiepileptic drugs (ED-BoM-AED)—a prospective multicenter study. Epilepsy Res. 2013; 106:417–22. doi: 10.1016/j.eplepsyres.2013.06.020 23916144
Článok vyšiel v časopise
PLOS One
2019 Číslo 11
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Dlouhodobá recidiva a komplikace spojené s elektivní operací břišní kýly
Najčítanejšie v tomto čísle
- A daily diary study on maladaptive daydreaming, mind wandering, and sleep disturbances: Examining within-person and between-persons relations
- A 3’ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction
- A substitution mutation in a conserved domain of mammalian acetate-dependent acetyl CoA synthetase 2 results in destabilized protein and impaired HIF-2 signaling
- Molecular validation of clinical Pantoea isolates identified by MALDI-TOF