The Association Between Serum GGT Level and Bone Mineral Density in Postmenopausal Women

Heung Yeol Kim; Eun Hee Kong

doi:10.7180/kmj.2013.28.1.35

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Kim and Kong: The Association Between Serum GGT Level and Bone Mineral Density in Postmenopausal Women

Original Article

Kosin Medical Journal 2013;28(1):35-41.

Published online: 19 January 2013

DOI: https://doi.org/10.7180/kmj.2013.28.1.35

The Association Between Serum GGT Level and Bone Mineral Density in Postmenopausal Women

Heung Yeol Kim¹, Eun Hee Kong²

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 19 October 20126 December 2012 Accepted 2 January 2013

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.

Abstract

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.

Keywords: Bone mineral density, Gamma-glutamyl transferase, Postmenopause

REFERENCES

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.

2.Han M. Metabolic Syndrome Emerging from Menopause. J Korean Soc Menopause. 2011. 17:127–35.

3.Hofbauer LC., Schoppet M. Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases. JAMA. 2004. 292:490–5.

4.Khosla S., Riggs BL. Pathophysiology of age-related bone loss and osteoporosis. Endocrinol Metab Clin North Am. 2005. 34:1015–30. xi.

5.Lee DH., Blomhoff R., Jacobs DR Jr. Is serum gamma glutamyltransferase a marker of oxidative stress? Free Radic Res. 2004. 38:535–9.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

30.Glantzounis GK., Tsimoyiannis EC., Kappas AM., Galaris DA. Uric acid and oxidative stress. Curr Pharm Des. 2005. 11:4145–51.

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.

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.

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.

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)	P-value
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

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