Skip Navigation
Skip to contents

KMJ : Kosin Medical Journal

OPEN ACCESS
SEARCH
Search

Articles

Page Path
HOME > Kosin Med J > Volume 28(1); 2013 > Article
Original Article
The Association Between Serum GGT Level and Bone Mineral Density in Postmenopausal Women
Heung Yeol Kim1, Eun Hee Kong2
Kosin Medical Journal 2013;28(1):35-41.
DOI: https://doi.org/10.7180/kmj.2013.28.1.35
Published online: January 19, 2013

1Department of Obstetrics and Gynecology, College of Medicine, Kosin University, Busan, Korea

2Department of Family Medicine, College of Medicine, Kosin University, Busan, Korea

Corresponding author: Eun Hee Kong, Department of Family Medicine, Kosin University College of Medicine, #34, Amnam-dong, Seo-gu, Busan, 602-702, Korea TEL: 051-990-6365 FAX: 051-990-3045 E-mail: eh-kong@kosin.ac.kr
• Received: October 19, 2012   • Accepted: January 2, 2013

Copyright © 2013 Kosin University School of Medicine Proceedings

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • 1,193 Views
  • 1 Download
  • 2 Crossref
  • Objectives
    The aim of this study was to identify the relationship between serum gamma-glutamyltransferase (GGT) and bone mineral density (BMD) in postmenopausal women.
  • Methods
    We evaluated 200 postmenopausal women who were visiting a health promotion center at a university hospital from January 2009 to December 2011. Their current medical diseases and medication history were collected through medical records. Basic physical examinations and laboratory tests were performed on all subjects.
  • Results
    The levels of serum GGT within their normal range were positively correlated with waist circumference (P = 0.01), triglycerides (P <0.001), alkaline phosphatase (P = 0.009), and uric acid (P = 0.01). The serum GGT within their normal range were negatively associated with the femur neck BMD (P = 0.002). In adjusted analysis including age and body mass index, the BMD of the femur neck was more strongly associated with a high-normal serum GGT level among the postmenopausal women as compared with those with a low-normal serum GGT level (P = 0.02).
  • Conclusions
    Serum GGT within its normal range is negatively correlated with the BMD in the femur neck among postmenopausal women. It can be useful for selecting a group that is at high risk for the bone fracture regardless of the underlying mechanism.
Table 1.
General characteristics. (N=200)
Characteristics Mean ± SD
Age, y 57.71 ± 6.29
Weight, kg 59.14 ± 8.12
Height, cm 156.38 ± 5.28
BMI, kg/m2 24.19 ± 3.23
WC, cm 80.22 ± 8.23
SBP, mmHg DBP, mmHg 125.99 ± 16.35 76.70 ± 10.00
Glucose, mg/dL 94.09 ± 21.16
T-C, mg/dL HDL-C, mg/dL 206.00 ± 36.71 53.09 ± 12.56
LDL-C, mg/dL 135.82 ± 17.34
TG, mg/dL 119.91 ± 60.19
ALP, mg/dL 66.81 ± 19.83
GGT, mg/dL 18.71 ± 9.53
Uric acid, mg/dL 4.48 ± 0.91
Calcium, mg/dL 9.35 ± 0.38
Phosphate, mg/dL 3.74 ± 0.56
Hs-CRP, mg/dL 0.17 ± 0.52
F-BMD, T-score (SD) -1.53 ± 1.47
L-BMD, T-score (SD) -1.97 ± 1.07

cholesterol, HDL-C: high density lipoprotein cholesterol, LDL-C: low density lipoprotein cholesterol TG: triglyceride, ALP: alkaline phosphatase, GGT: gamma-glutamyl transferase, Hs-CRP: high sensitivity C-reactive protein, F-BMD: bone mineral density of Femur neck, L-BMD: bone mineral density of Lumbar spine (L1~L4).

Table 2.
Association with biochemical markers by the quartile of normal serum GGT levels.
Quartile of normal serum GGT levels (mg/dL) P-value
Q1 (4~12) (N = 50) Q2 (13~15) (N = 50) Q3 (16~23) (N = 50) Q4 (24~50) (N = 50)
Age, y 57.02 ± 6.24 56.55 ± 5.52 58.75 ± 6.49 58.50 ± 6.71 0.17
Weight, kg 57.76 ± 7.40 58.13 ± 7.81 59.75 ± 7.86 60.86 ± 9.12 0.15
Height, cm 156.72 ± 5.45 156.54 ± 5.52 156.16 ± 4.70 156.13 ± 5.55 0.91
BMI, kg/m2 23.50 ± 2.66 23.76 ± 3.40 24.52 ± 3.14 24.97 ± 3.52 0.06
WC, cm 78.55 ± 7.24 78.27 ± 8.20 81.54 ± 7.68 82.46 ± 9.06 0.01
SBP, mmHg 123.29 ± 15.69 125.65 ± 12.96 124.59 ± 17.27 130.38 ± 18.44 0.11
DBP, mmHg 74.93 ± 10.97 76.85 ± 8.75 76.48 ± 9.51 78.52 ± 10.56 0.30
Glucose, mg/dL 91.45 ± 23.28 93.31 ± 16.72 92.61 ± 13.72 98.91 ± 27.77 0.25
T-C, mg/dL 197.47 ± 37.33 205.87 ± 37.61 209.20 ± 36.21 211.31 ± 35.13 0.20
HDL-C, mg/dL 52.20 ± 11.42 55.60 ± 15.58 52.88 ± 11.39 51.73 ± 11.35 0.37
LDL-C, mg/dL 131.48 ± 11.42 132.45 ± 15.58 134.23 ± 11.39 135.71 ± 11.35 0.35
TG, mg/dL 107.75 ± 45.65 107.78 ± 47.28 113.91 ± 42.96 149.77 ± 85.04 < 0.001
ALP, mg/dL 61.58 ± 15.00 63.36 ± 18.77 69.41 ± 22.77 72.73 ± 20.31 0.009
Uric acid, mg/dL 4.23 ± 0.81 4.34 ± 0.85 4.62 ± 0.78 4.73 ± 1.09 0.01
Calcium, mg/dL 9.31 ± 0.36 9.34 ± 0.36 9.36 ± 0.40 9.38 ± 0.41 0.79
Phosphate, mg/dL 3.67 ± 0.42 3.71 ± 0.45 3.75 ± 0.53 3.78 ± 0.43 0.47
Hs-CRP, mg/dL 0.15 ± 0.19 0.12 ± 0.13 0.25 ± 0.95 0.18 ± 0.36 0.59
F-BMD, T-score (SD) -1.16 ± 1.60 -1.24 ± 1.41 -1.35 ± 1.56 -1.64 ± 1.29 0.002
L-BMD, T-score (SD) -1.71 ± 1.13 -1.62 ± 1.05 -2.45 ± 1.07 -2.13 ± 1.03 0.33

Data shown are mean ± SD Note: P-value by one way ANOVA analysis

Table 3.
Association with biochemical markers by the BMD T-scores of femur neck
Bone mineral density of femur neck
P-value
T-score ≥ -1.0 -2.5 < T-score < -1.0 T-score ≤ -2.5
(N = 103) (N = 66) (N = 31)
Age, y 54.49 ± 4.46 57.09 ± 5.13 61.55 ± 6.90 < 0.001
Weight, kg 60.29 ± 8.63 60.559 ± 7.55 56.57 ± 7.62 0.003
Height, cm 157.28 ± 5.19 156.72 ± 5.12 155.16 ± 5.38 0.04
BMI, kg/m2 24.39 ± 3.47 24.68 ± 3.12 23.50 ± 3.01 0.06
WC, cm 79.54 ± 9.18 80.39 ± 7.03 80.72 ± 8.40 0.66
SBP, mmHg 124.62 ± 17.07 124.28 ± 13.26 129.07 ± 18.09 0.13
DBP, mmHg 76.24 ± 11.00 75.72 ± 9.348 78.15 ± 9.538 0.29
Glucose, mg/dL 93.38 ± 23.46 92.46 ± 12.59 96.42 ± 25.26 0.49
T-C, mg/dL 209.41 ± 35.33 203.10 ± 35.57 205.49 ± 39.31 0.57
HDL-C, mg/dL 53.96 ± 11.73 52.01 ± 13.98 53.31 ± 11.94 0.63
LDL-C, mg/dL 129.48 ± 10.42 134.51 ± 15.38 130.23 ± 12.79 0.53
TG, mg/dL 120.30 ± 47.96 115.89 ± 57.50 123.54 ± 73.02 0.74
ALP, mg/dL 62.80 ± 18.35 67.20 ± 17.21 70.43 ± 22.97 0.06
GGT, mg/dL 14.26 ± 10.40 19.31 ± 10.39 25.57 ± 7.54 < 0.001
Uric acid, mg/dL 4.38 ± 0.83 4.52 ± 0.80 4.55 ± 1.07 0.50
Calcium, mg/dL 9.32 ± 0.34 9.38 ± 0.40 9.35 ± 0.41 0.59
Phosphate, mg/dL 3.71 ± 0.42 3.74 ± 0.45 3.77 ± 0.53 0.45
Hs-CRP, mg/dL 0.22 ± 0.83 0.13 ± 0.16 0.16 ± 0.31 0.62

Data shown are mean ± SD

Note: P-value by one way ANOVA analysis

Table 4.
Multiple linear regression analysis for associated biochemical markers of BMD T-score of femur neck
Variables B Standard error Beta P-value
WC, cm -0.019 0.01 -0.146 0.16
SBP, mmHg 0.004 0.008 0.062 0.58
DBP, mmHg -0.003 0.01 -0.024 0.82
Glucose, mg/dL 0.002 0.003 0.031 0.62
T-C, mg/dL 0.001 0.002 0.048 0.46
HDL-C, mg/dL -0.002 0.006 -0.027 0.70
LDL-C, mg/dL -0.023 0.006 -0.037 0.65
TG, mg/dL -0.002 0.001 -0.125 0.08
ALP, mg/dL -0.004 0.003 -0.076 0.22
GGT, mg/dL 0.115 0.007 0.324 0.02
Uric acid, mg/dL -0.019 0.07 -0.016 0.81
Calcium, mg/dL -0.208 0.17 -0.075 0.23
Phosphate, mg/dL -0.117 0.15 -0.076 0.41
Hs-CRP, mg/dL 0.003 0.12 0.001 0.98
(constant) 0.893 2.73 0.74

Note: P-value from multiple linear regression analysis. Adjusted by age and BMI.

Table 5.
Multiple linear regression analysis for associated biochemical markers of BMD T-score of lumbar spine (L1~L4)
Variables B Standard error Beta P-value
WC, cm -0.005 0.01 -0.028 0.79
SBP, mmHg 0.002 0.01 0.024 0.83
DBP, mmHg -0.002 0.01 -0.010 0.92
Glucose, mg/dL 0.007 0.005 0.099 0.12
T-C, mg/dL 0.002 0.003 0.059 0.37
HDL-C, mg/dL 0.006 0.009 0.053 0.70
LDL-C, mg/dL 0.016 0.009 0.043 0.62
TG, mg/dL -0.001 0.002 -0.048 0.51
ALP, mg/dL -0.010 0.005 -0.136 0.03
GGT, mg/dL 0.008 0.01 0.052 0.41
Uric acid, mg/dL 0.044 0.11 0.027 0.69
Calcium, mg/dL 0.009 0.24 0.002 0.97
Phosphate, mg/dL 0.006 0.32 0.003 0.65
Hs-CRP, mg/dL -0.062 0.16 -0.022 0.71
(constant) -3.203 3.82 0.40

Note: P-value from multiple linear regression analysis. Adjusted by age and BMI

  • 1.Kanis JA, Oden A, Johansson H, Borgstrom F, Strom O, McCloskey E. FRAX and its applications to clinical practice. Bone 2009;44:734–43.ArticlePubMed
  • 2.Han M. Metabolic Syndrome Emerging from Menopause. J Korean Soc Menopause 2011;17:127–35.Article
  • 3.Hofbauer LC, Schoppet M. Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases. JAMA 2004;292:490–5.ArticlePubMed
  • 4.Khosla S, Riggs BL. Pathophysiology of age-related bone loss and osteoporosis. Endocrinol Metab Clin North Am 2005;34:1015–30. xi..ArticlePubMed
  • 5.Lee DH, Blomhoff R, Jacobs DR Jr. Is serum gamma glutamyltransferase a marker of oxidative stress? Free Radic Res 2004;38:535–9.PubMed
  • 6.Strasak AM, Rapp K, Brant LJ, Hilbe W, Gregory M, Oberaigner W, et al. Association of gamma-glutamyltransferase and risk of cancer incidence in men: a prospective study. Cancer Res 2008;68:3970–7.ArticlePubMedPMC
  • 7.Ryu S, Chang Y, Kim DI, Kim WS, Suh BS. gamma-Glutamyltransferase as a predictor of chronic kidney disease in nonhypertensive and nondiabetic Korean men. Clin Chem 2007;53:71–7.PubMed
  • 8.Lim J, Kim S, Ke S, Cho B. The Prevalence of Obesity, Abdominal Obesity and Metabolic Syndrome among Elderly in General Population. Korean J Fam Med 2011;32:128–34.Article
  • 9.Sheng Z, Xu K, Ou Y, Dai R, Luo X, Liu S, et al. Relationship of body composition with prevalence of osteoporosis in central south Chinese postmenopausal women. Clin Endocrinol (Oxf) 2011;74:319–24.ArticlePubMed
  • 10.Lee JY, Jeong KA, Cha YJ, Kim HY. The Relationship between Body Composition, Serum Lipid Profile and Bone Mineral Density in Korean Women. Osteoporosis 2009;7:159–67.
  • 11.Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Nagata Y. Relationship between body fat distribution and bone mineral density in premenopausal Japanese women. Obstet Gynecol 2000;95:722–5.ArticlePubMed
  • 12.Sowers MF, Kshirsagar A, Crutchfield MM, Updike S. Joint influence of fat and lean body composition compartments on femoral bone mineral density in premenopausal women. Am J Epidemiol 1992;136:257–65.ArticlePubMed
  • 13.Oh HJ, Jeong MH, Kim HY, Oh JY, Jung JY, Kim MH, et al. The Effect of Hormone Replacement Therapy on Bone Mineral Density in Korean Postmenopausal Women for 2 Years. Osteoporosis 2009;7:35–42.
  • 14.Salim A, Nacamuli RP, Morgan EF, Giaccia AJ, Longaker MT. Transient changes in oxygen tension inhibit osteogenic differentiation and Runx2 expression in osteoblasts. J Biol Chem 2004;279:40007–16.ArticlePubMed
  • 15.Arnett TR, Gibbons DC, Utting JC, Orriss IR, Hoebertz A, Rosendaal M, et al. Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol 2003;196:2–8.ArticlePubMed
  • 16.Galli F, Piroddi M, Annetti C, Aisa C, Floridi E, Floridi A. Oxidative stress and reactive oxygen species. Contrib Nephrol 2005;149:240–60.ArticlePubMed
  • 17.Altindag O, Erel O, Soran N, Celik H, Selek S. Total oxidative/anti-oxidative status and relation to bone mineral density in osteoporosis. Rheumatol Int 2008;28:317–21.ArticlePubMed
  • 18.Basu S, Michaëlsson K, Olofsson H, Johansson S, Melhus H. Association between Oxidative Stress and Bone Mineral Density. Biochem Biophys Res Commun 2001;288:275–9.ArticlePubMed
  • 19.Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR. Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 1990;85:632–9.ArticlePubMedPMC
  • 20.Dreher I, Schutze N, Baur A, Hesse K, Schneider D, Kohrle J, et al. Selenoproteins are expressed in fetal human osteoblast-like cells. Biochem Biophys Res Commun 1998;245:101–7.ArticlePubMed
  • 21.Sontakke AN, Tare RS. A duality in the roles of reactive oxygen species with respect to bone metabolism. Clin Chim Acta 2002;318:145–8.ArticlePubMed
  • 22.Maggio D, Barabani M, Pierandrei M, Polidori MC, Catani M, Mecocci P, et al. Marked decrease in plasma antioxidants in aged osteoporotic women: results of a cross-sectional study. J Clin Endocrinol Metab 2003;88:1523–7.ArticlePubMed
  • 23.Borud O, Mortensen B, Mikkelsen IM, Leroy P, Wellman M, Huseby NE. Regulation of gamma-glutamyltransferase in cisplatin-resistant and -sensitive colon carcinoma cells after acute cisplatin and oxidative stress exposures. Int J Cancer 2000;88:464–8.ArticlePubMed
  • 24.Lee DH, Jacobs DRJ, Gross M, Kiefe CI, Roseman J, Lewis CE, et al. Gamma-glutamyltransferase is a predictor of incident diabetes and hypertension: the coronary artery risk development in young adults (CARDIA) study. Clin Chem 2003;49:1358–66.PubMed
  • 25.Allen JP, Litten RZ, Fertig JB, Sillanaukee P. Carbohydrate-deficient transferrin, gamma-glutamyltransferase, and macrocytic volume as biomarkers of alcohol problems in women. Alcohol Clin Exp Res 2000;24:492–6.ArticlePubMed
  • 26.Iwasaki T, Yoneda M, Kawasaki S, Fujita K, Nakajima A, Terauchi Y. Hepatic fat content-independent association of the serum level of gamma-glutamyltransferase with visceral adiposity, but not subcutaneous adiposity. Diabetes Res Clin Pract 2008;79:e13–4.Article
  • 27.Verrijken A, Francque S, Mertens I, Talloen M, Peiffer F, Van Gaal L. Visceral adipose tissue and inflammation correlate with elevated liver tests in a cohort of overweight and obese patients. Int J Obes (Lond) 2010;34:899–907.ArticlePubMed
  • 28.Yamada J, Tomiyama H, Yambe M, Koji Y, Motobe K, Shiina K, et al. Elevated serum levels of alanine aminotransferase and gamma glutamyltransferase are markers of inflammation and oxidative stress independent of the metabolic syndrome. Atherosclerosis 2006;189:198–205.ArticlePubMed
  • 29.Yu MA, Sanchez-Lozada LG, Johnson RJ, Kang DH. Oxidative stress with an activation of the renin-angiotensin system in human vascular endothelial cells as a novel mechanism of uric acid-induced endothelial dysfunction. J Hypertens 2010;28:1234–42.ArticlePubMed
  • 30.Glantzounis GK, Tsimoyiannis EC, Kappas AM, Galaris DA. Uric acid and oxidative stress. Curr Pharm Des 2005;11:4145–51.ArticlePubMed
  • 31.Bonora E, Capaldo B, Perin PC, Del Prato S, De Mattia G, Frittitta L, et al. Hyperinsulinemia and insulin resistance are independently associated with plasma lipids, uric acid and blood pressure in non-diabetic subjects. The GISIR database. Nutr Metab Cardiovasc Dis 2008;18:624–31.ArticlePubMed
  • 32.Lippi G, Montagnana M, Luca Salvagno G, Targher G, Cesare Guidi G. Epidemiological association between uric acid concentration in plasma, lipoprotein(a), and the traditional lipid profile. Clin Cardiol 2010;33:E76–80.ArticlePMC
  • 33.Machin M, Simoyi MF, Blemings KP, Klandorf H. Increased dietary protein elevates plasma uric acid and is associated with decreased oxidative stress in rapidly-growing broilers. Comp Biochem Physiol B Biochem Mol Biol 2004;137:383–90.ArticlePubMed

Figure & Data

References

    Citations

    Citations to this article as recorded by  
    • The Role of Vitamin D in Menopausal Medicine
      Mijin Kim, Tae-Hee Kim, Hae-Hyeog Lee, Heung Yeol Kim, Min-Jung Oh
      Kosin Medical Journal.2016; 31(2): 97.     CrossRef
    • The Role of Vitamin D in Menopausal Medicine
      Mijin Kim, Tae-Hee Kim, Hae-Hyeog Lee, Heung Yeol Kim, Min-Jung Oh
      Kosin Medical Journal.2016; 31(2): 97.     CrossRef

    • PubReader PubReader
    • ePub LinkePub Link
    • Cite
      CITE
      export Copy
      Close
    • Download Citation
      Download Citation
      Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

      Format:
      • RIS — For EndNote, ProCite, RefWorks, and most other reference management software
      • BibTeX — For JabRef, BibDesk, and other BibTeX-specific software
      Include:
      • Citation for the content below
      The Association Between Serum GGT Level and Bone Mineral Density in Postmenopausal Women
      Kosin Med J. 2013;28(1):35-41.   Published online January 19, 2013
      Close
    • XML DownloadXML Download

    KMJ : Kosin Medical Journal