Gynecological Endocrinology

ISSN: 0951-3590 (Print) 1473-0766 (Online) Journal homepage: http://www.tandfonline.com/loi/igye20

Association of serum leptin with bone mineral

density in postmenopausal osteoporotic females

Saba Tariq, Mukhtiar Baig, Sundus Tariq & Muhammad Shahzad

To cite this article: Saba Tariq, Mukhtiar Baig, Sundus Tariq & Muhammad Shahzad (2016):
Association of serum leptin with bone mineral density in postmenopausal osteoporotic
females, Gynecological Endocrinology, DOI: 10.1080/09513590.2016.1261103

To link to this article: http://dx.doi.org/10.1080/09513590.2016.1261103

Published online: 23 Dec 2016.

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ISSN: 0951-3590 (print), 1473-0766 (electronic)

Gynecol Endocrinol, Early Online: 1–5

! 2016 Informa UK Limited, trading as Taylor & Francis Group. DOI: 10.1080/09513590.2016.1261103

ORIGINAL ARTICLE

Association of serum leptin with bone mineral density in

postmenopausal osteoporotic females
Saba Tariq1,2, Mukhtiar Baig3, Sundus Tariq4,5, and Muhammad Shahzad2
1
Department of Pharmacology, University Medical and Dental College, Faisalabad, Pakistan, 2Department of Pharmacology, University of Health
Sciences, Lahore, Pakistan, 3Department of Clinical Biochemistry, Faculty of Medicine, Rabigh, King Abdulaziz University, Jeddah, Saudi Arabia,
4
Department of Physiology, University Medical and Dental College, Faisalabad, Pakistan, and 5Department of Physiology, University of Health
Sciences, Lahore, Pakistan

Abstract Keywords
Objective: Present study was designed to find out whether leptin is a predictor of bone mass BMD, BMI, Osteoporosis, serum leptin
density (BMD) in premenopausal women (PMW) and postmenopausal osteoporotic women
(PMOPW) or it has no association with BMD. History
Methods: One hundred and ninety two women (98 PMOPW and 94 PMW) were recruited for this
study. The control group was BMI matched with osteoporotic subjects. BMD assessment was Received 28 July 2016
done on calcaneus by peripheral ultrasound bone densitometry and T scores were determined. Revised 15 October 2016
Serum leptin levels were measured by enzyme-linked immunosorbent assay (ELISA). Accepted 25 October 2016
Results: Serum leptin and BMD values were significantly different in both groups (leptin, Published online 21 December 2016
18.56 ± 8.65 ng/ml versus 21.64 ± 9.80 ng/ml, p ¼ 0.02) and (BMD, 0.70 ± 0.19 versus
3.17 ± 0.59, p ¼ 0.000), respectively. In PMOPW serum leptin and BMD were considerably
correlated with weight (lep, r ¼ 0.53, p ¼50.001; BMD, r ¼ 0.21, p ¼ 0.02), BMI (lep, r ¼ 0.52,
p ¼50.001; BMD, r ¼ 0.27, p ¼ 0.005), waist circumference (lep, r ¼ 0.61, p ¼50.001; BMD,
r ¼ 0.18, p ¼ 0.04), hip circumference (lep, r ¼ 0.58, p ¼50.001).
Multivariate linear stepwise regression analysis showed that weight and BMI in PMW and
PMOPW were independent predictors of BMD. Serum leptin level was not found to be the
predictor of BMD in both groups.
Conclusion: The present results indicate that body weight and BMI have an impact on BMD
while serum leptin is not associated with BMD in PMW and PMOPW.

Introduction which can inhibit adipogenesis discrimination of BMSC. It can

excite discrimination of osteoblasts while another study has
Leptin is an important member of adipokine family that helps in
pointed out that extremely elevated levels of leptin cause
regulation of food intake, energy homeostasis, reproduction,
apoptosis of BMSC. The proliferation of cultured human osteo-
metabolism, immune function, bone physiology, tissue remodel-
blasts are also stimulated with leptin, and it causes human BMSC
ing, neuroendocrine functions and others [1]. Research has shown
to express collagen-I, osteocalcin and alkaline phosphatase and
that the leptin plays a significant role in the control of body
matrix mineralization [6].
weight and regulation of bone density. Bone mass has been said to
A study in Caucasian women demonstrated that serum leptin
be regulated by leptin. The interaction of leptin with bone is
had an inverse relationship with bone mass density (BMD), while
multifaceted. It also depends on the fact that whether leptin has a
another study observed a positive connection [7]. A large-scale
direct action on osteoblasts through receptors or it acts indirectly
study established that serum leptin has no association with BMD
through the hypothalamus; it can both stimulate and inhibit bone
[8]. Similarly, in another study no relation has been established
formation [2]. Reduction in serum leptin levels is linked with
between leptin and BMD [9].
decreased intake of food, which might result in a reduction in the
The effects of serum leptin on bone metabolism are incon-
formation of bone and growth, especially in children and
sistent and complicated, so there is still need to explore the
adolescence [3]. In mice, lack of leptin also causes loss of bone
association of leptin with BMD. Therefore, the present study was
and increased adiposity in bone marrow [4].
designed to find out whether leptin is a predictor of BMD in
Leptin has direct effects on bone by inhibiting the bone
premenopausal women (PMW) and postmenopausal osteoporotic
marrow stromal cells (BMSC) to generate osteoclast while
women (PMOPW) or it has no association with BMD.
stimulating them to differentiate into osteoblasts [5]. The
BMSC can be discriminated mainly into adipocytes or osteoblast
cell family. These adipocytes in bone marrow provide leptin, Subjects and methods
Institutional Ethical Review Board gave the approval to conduct
Address for correspondence: Muhammad Shahzad, Department of this study according to Helsinki Declaration of human rights.
Pharmacology, University of Health Sciences, Lahore 54600, Pakistan. All participants in the study gave their written informed consent.
Tel: +00923346061838. E-mail: shahzad912@hotmail.com This cross-sectional study was conducted at the Pharmacology
2 S. Tariq et al. Gynecol Endocrinol, Early Online: 1–5

Department, Shaikh Zayed Postgraduate Medical Institute, Shaikh validity of the model. The significance was set at the p50.05 for
Zayed Hospital, Lahore, Pakistan. The samples were collected all tests.
from Orthopedic OPD of Shaikh Zayed Hospital, Lahore,
Pakistan. The sampling technique employed was purposive Results
nonrandomized.
The comparison of the baseline characteristics of the PMW and
A total of 500 subjects were assessed for eligibility for
PMOPW are given in Table 1. Serum leptin and BMD values were
inclusion in the study and ninety-eight newly diagnosed, untreated
significantly different in both groups (leptin, 18.56 ± 8.65 ng/ml
PMOPW (having LMP 43 years, with T-Score52.5) were
versus 21.64 ± 9.80 ng/ml, p ¼ 0.03) and (BMD, 0.70 ± 0.19
enrolled and ninety-four, BMI-matched PMW (having regular
versus 3.17 ± 0.59, p50.001) respectively. However, no sig-
menses, with T-Score41) were selected as a control group. The
nificant difference observed in the mean value of age, body
osteoporosis was labeled according to World Health Organization
weight, height, BMI, waist and hip circumference, serum calcium
(WHO) criterion that is ‘‘BMD measurements in women that fall
and age of menarche.
more than 2.5 standard deviations (SD) below the young mean’’
Table 2 showing correlation of leptin and BMD with other
[10].
variables in PMW. Serum leptin and BMD were considerably
All subjects in our study were Pakistani and of the same origin.
correlated with weight (lep, r ¼ 0.42, p ¼50.001; BMD,
We collected all samples from one public sector hospital and
r ¼ 0.21, p ¼0.02), BMI (lep, r ¼ 0.41, p ¼50.001; BMD,
people coming to that hospital are mostly from the lower
r ¼ 0.25, p ¼0.007), waist circumference (lep, r ¼ 0.59,
socioeconomic class. A detailed history was taken from all
p ¼50.001), hip circumference (lep, r ¼ 0.46, p ¼50.001;BMD,
subjects about menarche, menopause, any disease and fracture
r ¼ 0.19, p ¼50.03). After adjusting age, body weight and waist
history. All subjects’ height, weight, waist and hip circumferences
circumference the correlation of BMI with serum leptin and BMD
were measured. The participants were excluded if they had heart
was lost (lep, r ¼ 0.065, p ¼ 0.26; BMD, r ¼ 0.159, p ¼ 0.06),
diseases (myocardial infarction), diabetes mellitus, epilepsy,
and correlation of hip circumference remained significant with
malignancies, osteomalacia, thyroid and gastrointestinal disease.
leptin (lep, r ¼ 0.49, p ¼50.001). However, no correlation
The participants were also excluded from the study if they were
between serum leptin and BMD was observed before and after
receiving medications such as corticosteroids, estrogen therapy,
adjusting several variables.
androgen, selective estrogen receptor modulators, calcitonin,
Similarly Table 2 is also showing correlation of leptin and
PTH, calcium, vitamin D and bisphosphonates.
BMD with other variables in PMOPW. Serum leptin and BMD
From PMW and PMOPW blood samples were taken early in
were considerably correlated with weight (lep, r ¼ 0.53,
the morning (12–14 h fasting), and after centrifugation, all
p ¼50.001; BMD, r ¼ 0.21, p ¼0.02), BMI (lep, r ¼ 0.52,
samples were stored at 70  C for analysis of serum calcium
p ¼50.001; BMD, r ¼ 0.27, p ¼0.005), waist circumference
and leptin.
(lep, r ¼ 0.61, p ¼50.001; BMD, r ¼ 0.18, p ¼ 0.04), hip circum-
Leptin levels were measured by enzyme-linked immunosorb-
ference (lep, r ¼ 0.58, p ¼50.001). After adjusting age, body
ent assay (ELISA) supplied by Axis-Shield Diagnostics Limited,
weight and waist circumference the correlation of BMI with
Dundee, United Kingdom. The sensitivity of leptin kit (lowest
serum leptin and BMD was lost (lep, r ¼ 0.09, p ¼ 0.18; BMD,
detectable limit) was 0.1 ng per milliliter and Intra- and interassay
r ¼ 0.16, p ¼ 0.06), and correlation of hip circumference
coefficients of variations were 4.3% and 5.8%, respectively.
become insignificant with leptin (r ¼ 0.10, p ¼ 0.15). However,
Serum calcium levels were determined by calcium colorimetric
no correlation between serum leptin and BMD was observed
assay manufactured by Fluitest CaCPC Analytic on
before and after adjusting several variables.
Biotechnologies AG, Germany. The intraassay and interassay
Table 3 shows the parameters identified as significant and
coefficient of variation were 1.59% for calcium. The lower
independent predictors of BMD using the multiple linear stepwise
detection limit was 0.01 mmol/I (0.04 mg/dl).
regression analysis. The independent predictors of BMD were
The peripheral ultrasound bone densitometry was done to
weight and BMI in PMW and PMOPW, which explained 5.8%,
measure BMD on the calcaneus (heel). We used QUS because of
and 7.5% of the variance in PMW and 4.5%, and 6.4% of the
its abilities to assess the fracture risk similar to that of DEXA,
variance in PMOPW, respectively. Several independent variables
and it is inexpensive, transportable and ionizing radiation free
were included in the regression analysis models including BMI,
[11–13].
body weight, waist and hip circumference.

Statistical analysis
The collected data was analyzed on SPSS 16.0 (Statistical Table 1. Comparison of basic parameters in PMW and PMOPW.
Package for Social Sciences, IBM, New York, NY). Pearson’s
correlation coefficients were calculated to estimate the relation- Parameters PMW (N ¼ 94) PMOPW (N ¼ 98)
ship of leptin with BMD and with anthropometric characteristics. Age 57.92 ± 4.31 58.42 ± 3.56
Age, body weight and waist circumference could be related with Height (m) 1.53±.07 1.53 ± 0.07
serum leptin and BMD levels, therefore, by taking these three as Weight (kg) 66.96 ± 13.64 67.08 ± 12.98
covariates, the partial correlations were calculated to explore the BMI (kg/m2) 28.67 ± 5.85 28.75 ± 5.56
correlation of BMD with leptin and other parameters. Waist circumference (inches) 38.97 ± 4.21 39.03 ± 4.24
Hip circumference (inches) 41.29 ± 4.97 41.40 ± 4.75
Independent t-test was used to compare levels of leptin and Waist_hip ratio 0.94 ± 0.07 .94 ± 0.07
BMD and other parameters in PMW and PMOPW. Leptin level (ng/ml) 18.56 ± 8.66 21.64 ± 9.80*
The stepwise multiple regression analysis was performed T score 0.70 ± 0.19 3.17±.59**
taking BMD as a dependent factor and body weight, and BMI and Calcium level (mg/dl) 8.63 ± 0.78 8.72 ± 0.79
waist and hip circumference entered as covariates to find out the Age of menarche 11.83 ± 1.14 11.72 ± 1.11
effects of these variables on BMD (because in the present study
Results are shown as mean ± standard deviation. *p50.03., **p50.001.
these variables were correlated with BMD). R square change that PMW: Premenopausal women; PMOPW: Postmenopausal osteoporotic
expressed the part of the variance of the dependent variable women.
elucidate by the covariates entered in the model represented the
DOI: 10.1080/09513590.2016.1261103 Relationship of Leptin & BMD 3

0.172 (0.051)

0.161 (0.064)

(0.053)
(0.031)
(0.191)
(0.070)
(0.362)
(0.244)
Table 3. Multivariate linear stepwise analysis showing independent

Adjusted r
(p values)
predictors of BMD in PMW and PMOPW.

0.170
0.197
0.093
0.156
0.037
0.074
PMW (N ¼ 94) PMOPW (N ¼98)

1
BMD Parameters b-coefficient r2 p values b-coefficient r2 p values
Weight (kg) 0.240 0.058 0.020 0.212 0.045 0.03
BMI (kg/m2) 0.274 0.075 0.007 0.245 0.064 0.01

0.267** (0.005)
0.213* (0.020)

0.184* (0.038)
Unadjusted r

0.007 (0.475)
0.066 (0.263)

0.143 (0.084)
0.031 (0.384)
0.152 (0.072)
0.079 (0.224)
0.006 (0.477)
0.063 (0.273)
(p values)
Dependent variable BMD, p50.05, PMW: Premenopausal women;
PMOPW: Postmenopausal osteoporotic women.

Discussion
PMOPW

The fat tissue interacts directly with the bone via a number of
cytokines like adiponectin, leptin and tumor necrosis factor-alpha,
0.097 (0.180)
0.077 (0.235)

(0.153)
(0.059)
(0.200)
(0.337)
(0.021)

(0.244)
which are fat derivatives. There are other fat related hormones,
Adjusted r
(p values)

which significantly affect bone metabolism such as vitamin D,

estrogen, androgens. Furthermore, parathyroid hormone, calci-
0.109
0.165
0.089
0.045
0.214

0.074 tonin, calcium, physical activity and increasing age also affect
1

bone metabolism [14,15]. Thus, final balance of bone deposition

Leptin

versus resorption affected by the activity of several factors and the

genetic predisposition of an individual to osteoporosis and
0.534** (50.001)
0.517** (50.001)
0.605** (50.001)
0.577** (50.001)

osteoarthritic changes [14].

Unadjusted r
(p values)
0.092 (0.190)
0.073 (0.242)

0.007 (0.474)
0.001 (0.498)
0.049 (0.319)
0.067 (0.261)

0.063 (0.273)

In present study, serum leptin level was not found to be the

predictor of BMD in both groups (PMW and PMOPW). Only
body weight and BMI were independent predictors of BMD in
Pearson’s correlation and partial correlation, in partial correlation adjusted variable were age, weight and waist circumference.

both groups. Our results regarding leptin are consistent with

1

several other studies [8,9,16] and incompatible with few others

[7,17]. Similar to our results, another study reported a significant
correlation between weight and BMI with BMD in femur neck
0.111 (0.142)

0.159 (0.062)

(0.252)
(0.190)
(0.456)
(0.118)
(0.450)
(0.237)
Adjusted r

and total hip, and a significant negative correlation between age

(p values)

and femur neck BMD, and in that study weight and BMI were
0.069
0.091
0.011
0.123
0.013
0.074

found to be the significant predictor of BMD [18].

1.00

In literature, numerous studies reported the positive associ-

ation between increased body weight and/or BMI with BMD or
BMD

even shielding result against osteoporosis and fractures [19–21].

This could be explained that elevated weight/BMI acts as a
0.212* (0.018)
0.248* (0.007)

0.190* (0.031)
0.087 (0.198)
0.033 (0.375)

0.101 (0.162)

0.163 (0.054)
0.035 (0.365)
0.132 (0.098)
0.010 (0.461)
Unadjusted r

011 (0.458)

heavier mechanical load on bones, which subsequently causes

(p values)

increased bone remodeling to resist this load [19,22]. In this

Table 2. Correlation of leptin and BMD with other variables in PMW and PMOPW.

regard, few other mechanisms may contribute such as increased

1.00

synthesis of estrogen, elevated secretion of insulin and increased

PMW: Premenopausal women; PMOPW: Postmenopausal osteoporotic women.

serum leptin levels [21]. Conversely, there are few other studies
showing a negative association of obesity with BMD and
PMW

proposed that it could be due to secretion of pro-inflammatory

0.498* (50.001)

cytokines that stimulate bone resorption [20], reduced adiponectin

0.033 (0.375)

0.065 (0.265)

0.047 (0.326)
0.054 (0.300)
0.041 (0.346)
0.063 (0.271)

0.074 (0.237)
Adjusted r
(p values)

levels and augmented levels of parathormone [21,23].

It has been demonstrated in the literature that increased BMI is
a protecting factor against excessive bone loss in aging, and
increased BMI is associated with a decreased rate of bone loss
[24]. A study in Turkish postmenopausal women reported that fat
Leptin

mass and body weight are the significant predictors of BMD [25].
Recently, Doventas 2014, have demonstrated that leptin is not
0.426* (50.001)
0.407* (50.001)

0.456* (50.001)
0.597 (50.001)

the predictor of BMD in obese and non-obese osteoporotic and

0.017 (0. 435)
Unadjusted r

0.034 (0.369)
0.028 (0.391)

0.154 (0.065)

0.036 (0.364)
0.093 (0.181)

0.011 (0.458)
(p values)

non-osteoporotic females [26]. Another study has demonstrated

that leptin is not the predictor of BMD in healthy Chinese adult
males, however, in contrast to our results, this study found that
1.00

age is an independent determinant factor of BMD while weight

and BMI were not the predictors of BMD but that study was
conducted in adult males [27].
The present study observed a significant positive correlation
Waist circumference
Hip circumference

between serum leptin and BMI in both groups. These are

Age of menarche

concurred with several other studies [9,28].

Waist-hip ratio
Calcium level

Serum leptin

The results of the present study regarding the relationship

Parameters

between leptin and BMD are consistent with several other

T score
Weight
Height

studies, which also found no correlation of leptin with BMD

LMP
BMI
Age

in either the osteoporotic or non-osteoporotic subjects [29–31].

4 S. Tariq et al.
The reason for these differences could be that leptin is secreted
both systemically as well as centrally. It’s systemic effects result
in enhanced BMD while its central effects result in decreased
BMD. The net effect would be an override or neutralization
depending on whichever drive central or peripheral was stronger
resulting in a negative, positive or no association with BMD
[16,17].
BMI is considered as one of the predictors of bone strength
and bone mineral density. A study stated that the common stromal
cell origin of both adipocyte and osteoblast could be the possible
link between bone tissue and fat tissue [30]. Researchers pointed
out that body weight plays an essential role in the determination
of osteoporosis [31]. In the current study, the mean BMI of the
subjects was in the pre-obesity category. The present study found
a significant correlation between weight and BMI with serum
leptin and with BMD. Our results were inconsistent with studies,
which have reported either decreased or increased value of total
BMD in relation to postmenopausal obesity, such as a study
concluded that an inverse association existed between fat and
bone mass after mechanical loading effects because of enhanced
body weight [32].
The results of previously published studies showed that
association of serum leptin and BMD is vague and it is suggested
that these contradictory results may be because of the different
ethnic groups under study, different dietary habits, lack of
physical activity and several other factors [16].
We did not find that leptin is a predictor of BMD in our study,
but it is directly related to body weight, and BMI and these are
also related with BMD. So it seems that leptin has no direct
relationship with BMD, but it may be postulated that it could
interact with BMD by some other mechanisms or factors.
Limitation
There are several limitations to our study, such as this is a cross-
sectional study, and BMD was measured by QUS while the
DEXA is the gold standard. A detailed history of physical activity
and caloric intake was not taken.
Conclusions
The present results indicate that body weight and BMI have an
impact on BMD while serum leptin is not associated with BMD in
Pakistani PMW and PMOPW. Further studies are recommended
to explore serum leptin and BMD relationship.
Acknowledgements
Special thanks to Prof. Dr. Khalid Parvez lone, Head Department of
Physiology and Cell Biology for providing lab facility to store and run the
samples.
Declaration of interest
The authors declare that they have no conflict of interest.
References
1. Stofkova A. Leptin and adiponectin: from energy and metabolic
dysbalance to inflammation and autoimmunity. Endocr Regul 2009;
43:157–68.
2. Hamrick MW, Della-Fera MA, Choi YH, et al. Injections of leptin
into rat ventromedial hypothalamus increase adipocyte apoptosis in
peripheral fat and in bone marrow. Cell Tissue Res 2007;327:
133–41.
3. Chan JL, Mantzoros CS. Role of leptin in energy-deprivation states:
normal human physiology and clinical implications for hypothal-
amic amenorrhoea and anorexia nervosa. Lancet 2005;366:74–85.
Gynecol Endocrinol, Early Online: 1–5
4. Hamrick MW, Pennington C, Newton D, et al. Leptin deficiency
produces contrasting phenotypes in bones of the limb and spine.
Bone 2004;34:376–83.
5. Holloway WR, Collier FM, Aitken CJ, et al. Leptin inhibits
osteoclast generation. J Bone Miner Res 2002;17:200–9.
6. Evans BAJ, Elford C, Gregory JW. Leptin control of bone
metabolism; direct or indirect action? Bone 2001; 128:149.
7. Kontogianni MD, Dafni UG, Routsias JG, et al. Blood leptin and
adiponectin as possible mediators of the relation between fat mass
and BMD in perimenopausal women. J Bone Miner Res 2004;19:
546–51.
8. Ruhl CE, Everhart JE. Relationship of serum leptin concentration
with bone mineral density in the United States population. J Bone
Miner Res 2002;17:1896–903.
9. Tariq S, Tariq S, Alam SS, et al. Effect of ibandronate treatment on
serum homocysteine and leptin in postmenopausal osteoporotic
females. Osteoporos Int 2015;26:1187–92.
10. World Health Organization Study Group on Assessment of Fracture
Risk and Its Application to Screening for Postmenopausal
Osteoporosis. Report of a WHO Study Group. Geneva, World
Health Organization, (Technical Report Series, No. 843), 1994.
11. Guglielmi G, Scalzo G. Imaging tools transform diagnosis of
osteoporosis: accurate and reproducible methods of quantifying
bone density can help predict fracture risk, determine therapeutic
intervention, and monitor response. Diagnostic Imaging Europe
2010;26:01–5.
12. Albanese CV, Terlizzi FD, Passariello R. Quantitative ultrasound of
the phalanges and DXA of the lumbar spine and proximal femur in
evaluating the risk of osteoporotic vertebral fracture in postmeno-
pausal women. Radiol Med 2011;116:92–101.
13. Brusin JH, Clung MC. Update on bone densitometry. Radiol
Technol 2009;81:153BD–70.
14. Jurimae J, Jurimae T. Adiponectin is a predictor of bone mineral
density in middle-aged premenopausal women. Osteoporos Int 2007;
18:1253–9.
15. Sanfélix-Gimeno G, Sanfelix-Genovés J, Hurtado I, Reig-Molla B,
Peiró S, et al. Vertebral fracture risk factors in postmenopausal
women over 50 in Valencia, Spain. A population-based cross-
sectional study. Bone 2013;52:393–9.
16. Wu N, Wang QP, Li H, et al. Relationships between serum
adiponectin, leptin concentrations and bone mineral density, and
bone biochemical markers in Chinese women. Clin Chim Acta 2010;
411:771–5.
17. Labouesse MA, Gertz ER, Piccolo BD, et al. Associations among
endocrine, inflammatory, and bone markers, body composition and
weight loss induced bone loss. Bone 2014;64:138–46.
18. Hoxha R, Islami H, Qorraj-Bytyqi H, et al. Relationship of weight
and body mass index with bone mineral density in adult men from
Kosovo. Mater Sociomed 2014;26:306–8.
19. Kang D, Liu Z, Wang Y, et al. Relationship of body composition
with bone mineral density in northern Chinese men by body mass
index levels. J Endocrinol Invest 2014;37:359–67.
20. Lloyd JT, Alley DE, Hawkes WG, et al. Body mass index is
positively associated with bone mineral density in US older adults.
Arch Osteoporos 2014;9:175.
21. Gonnelli S, Caffarelli C, Nuti R. Obesity and fracture risk. Clin
Cases Miner Bone Metab 2014;11:9–14.
22. Wee J, Sng BY, Shen L, et al. The relationship between body mass
index and physical activity levels in relation to bone mineral density
in premenopausal and postmenopausal women. Arch Osteoporos
2013;8:162.
23. Dogan A, Nakipoglu-Yüzer GF, Yildizgören MT, et al. Is age or the
body mass index (BMI) more determinant of the bone mineral
density (BMD) in geriatric women and men? Arch GerontolGeriatr
2010;51:338–41.
24. De Laet C, Kanis JA, Oden A, et al. Body mass index as a predictor
of fracture risk: a meta-analysis. Osteoporos Int 2005;16:1330–8.
25. Nur H, Toraman NF, Arica Z, et al. The relationship between body
composition and bone mineral density in postmenopausal Turkish
women. Rheumatol Int 2013;33:607–12.
26. Doventas A, Bolayirli IM, Incir S, et al. Interrelationships between
obesity and bone markers in post-menopausal women with either
obesity or osteoporosis. Eur Geriatr Med 2015;6:15–20. Available:
http://dx.doi.org/10.1016/j.eurger.2014.06.033.
27. Li XP, Zeng S, Wang M, et al. Relationships between serum
omentin-1, body fat mass and bone mineral density in healthy
DOI: 10.1080/09513590.2016.1261103
Chinese male adults in Changsha area. J Endocrinol Invest 2014;37:
991–1000.
28. Baig M, Rehman R, Tariq S, et al. Serum leptin levels in polycystic
ovary syndrome and its relationship with metabolic and hormonal
profile in Pakistani females. Int J Endocrinol 2014;2014: Article ID
132908, 5 pages. doi:10.1155/2014/132908.
29. Sebastia Ochoa A, Fernández-Garcı́a D, Reyes-Garcı́a, et al.
Adiponectin and leptin serum levels in osteoporotic postmenopausal
women treated with raloxifene or alendronate. Menopause 2012;19:
172–7.
Relationship of Leptin & BMD 5
30. Blum M, Harris SS, Must A, et al. Leptin, body composition and
bone mineral density in premenopausal women. Calcif Tissue Int
2003;73:27–32.
31. Zhao LJ, Jiang H, Papasian CJ, et al. Correlation of obesity and
osteoporosis: effect of fat mass on the determination of osteoporosis.
J Bone Min Res 2008;23:17–29.
32. Yamauchi M, Sugimoto T, Yamaguchi T, et al. Plasma leptin
concentrations are associated with bone mineral density and the
presence of vertebral fractures in postmenopausal women. Clin
Endocrinol 2001;55:341–7.