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Correlation between Reproductive 

Hormonal Level and Osteoporosis 

among Women in Mongolia 
 
 

Unentsatsral Lkhagvasuren1, 

Sarantuya Jav2, Battogtokh 

Zagdsuren3 

 
1Department of Obstetrics and 
Gynecology, Health Sciences, University 
of Mongolia, Ulaanbaatar, Mongolia; 
2Department of Molecular Biology and 
Genetics, Health Sciences, University of 
Mongolia, Ulaanbaatar, Mongolia; 
3Department of Kinesiology, University of 
Alabama, Alabama, USA 

 

 

 

 

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LKHAGVASUREN 

 

 

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Abstract 

Background: Postmenopausal osteoporosis is the most common bone metabolic disease associated with low bone mineral density 

(BMD) and osteopathic fragility fractures, which can lead to significant morbidity. The objective of this study was to investigate 

the relationship between serum follicle-stimulating hormone (FSH), luteinizing hormone (LH), and estradiol (E2) levels and bone 

mineral density (BMD) across the stages of menopause in Mongolian women.  

Methods: Two hundred sixty participants aged 50.1±4.4 years were enrolled in the study. Blood samples were obtained from each 

participant and analyzed using ELISA. Data were first stratified and analyzed by bone mineral density status (osteoporotic, 

osteopenic, and normal) and then by menopause status. Between group differences were analyzed using t-tests, and correlations 

were assessed using the Spearman rank order test, with Bonferonni correction. The data were analyzed using Statistical Package 

Statistical Software version 20.0 (SPSS Inc., Chicago, IL). Significance was set at p<0.05. 

Results: The mean menopausal age was 48.4±3.4, which is comparable to the Mongolian population mean menopausal age. The 

mean serum estradiol level in the normal BMD group was 18.3±13.1 pg/ml and  15.8±10.7 pg/ml in the osteoporotic group. The 

mean serum FSH in the normal BMD group was 54.5±44.1 pg/ml and 81.3±34.2 pg/ml in the osteoporotic group. The mean serum 

LH level in the normal BMD group was 53.1±41.2 and 75.1±26.1 pg/ml in the osteoporotic group. The mean T and Z score were 

lower in the osteoporotic group. FSH and LH levels significantly differed across menopause stages in that those who were post-

menopausal had higher levels compared to those who were pre- or peri-menopausal. Both hormones, FSH and LH, showed weak 

negative correlations with BMD level, but not E2. There were significant negative correlations between FSH and Speed of Sound 

(SOS) (r=-0.16; p<0.01), and  between osteoporosis with age (r=-0.30, p<0.05) and number of childbirths (r=-0.14 p<0.05).  

Discussion: Osteoporosis is a significant problem with associations to hormone levels in post-menopausal women. In our study, 

mean serum estradiol levels decreased with age, and the mean FSH and LH levels were higher in women of later menopausal stage. 

Further study is warranted to investigate the bone related studies to establish better statistical references among Mongolian women.  

Keywords: osteoporosis, post-menopausal women, reproductive hormone, menopause, Mongolia  

Correlation between Reproductive 

Hormonal Level and Osteoporosis 

among Women in Mongolia 

Unentsatsral Lkhagvasuren1, 

Sarantuya Jav2, Battogtokh 

Zagdsuren3 

 
1Department of Obstetrics and Gynecology, 
Health Sciences, University of Mongolia, 
Ulaanbaatar, Mongolia; 2Department of 
Molecular Biology and Genetics, Health 
Sciences, University of Mongolia, 
Ulaanbaatar, Mongolia; 3Department of 
Kinesiology, University of Alabama, 
Alabama, USA 

Research 

Postmenopausal osteoporosis is the most 

common bone metabolic disease associated with low 

bone mineral density (BMD) and osteopathic fragility 

fractures, which has been associated with significant 

disability and mortality.1 The majority of women spend 

one third of their lifetime in the postmenopausal period 

typically accompanied by an estrogen deficit state.2 The 

World Health Organization (WHO) defined osteoporosis 

as a reduction of 2.5 standard deviations in T-scores 

below the normal mean for young females at the age of 

peak bone mass.3 A T score between 1 to 2.5 SDs below 

average indicates osteopenia, which is a pre-osteoporotic 

state.3 The diagnostic measurement of Z-score indicates 

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the bone density relative to patients’ age and sex.4 A Z-

score below -2.0 is classified as below the expected range 

for that age, while above -2.0 is considered to be within 

the expected range for a given age.4,5 Worldwide, there 

are nearly 9 million osteoporotic fractures each year, 

generating a massive burden both to individuals and to 

health services.6 About 13-18% of women over the age 

of 50 years have osteoporosis and 37-50% have 

osteopenia in the USA.7 Unfortunately, no epidemiologic 

data have been published about the rate of osteoporosis 

in Mongolia. Anecdotal evidence suggests that rates in 

Mongolia are similar to those reported in the USA.  

 Low estradiol levels are a risk factor for 

osteoporosis and influences the quality of life for older 

women.8 Estrogen deficiency can lead to excessive bone 

re-absorption after menopause.9 To the best of our 

knowledge, there are no published studies on the 

relationship between serum reproductive hormonal level 

and BMD in postmenopausal women in Mongolia. 

Therefore, the purpose of this study is to evaluate the 

correlation between reproductive hormone levels such as 

follicle- stimulating hormone (FSH), luteinizing 

hormone (LH), estradiol (E2), and osteoporosis among 

postmenopausal women in Mongolia.  

Osteoporosis research is inadequate in 

Mongolia due to the lack of reliable diagnostic 

instruments and poor research infrastructure. Conducting 

such research is valuable to gerontology, endocrinology, 

and gynecology fields in Mongolia. Hence, the secondary 

purpose of this study is to establish a research database 

for future research in related fields.  

 

Methods 

Participants 

Two hundred sixty women with a mean age of 

50.1±4.4 years were included in the study. Participants 

were recruited from four districts from Ulaanbaatar City 

of Mongolia. All participants signed informed consents 

prior to study participation. The study was approved by 

the ethical committee of Health Sciences University of 

Mongolia.   

Participants were interviewed using a 

questionnaire developed by the investigators, which 

included demographics, body mass index (BMI), years 

since menopause, menarche age, menopause age, and 

health history. The participants were divided into three 

different groups based on their BMD value: osteoporosis, 

osteopenia, and normal. The mean age of the 

osteoporosis (T score: -2.5), osteopenia (T score: -2.5 to 

-1), and normal (T score: >-1) group was 54.0±3.9, 

51.5±4.3, and 48.5±3.8 years, respectively. The 

participants were further classified into four menopausal 

stages: premenopausal, perimenopausal, postmenopausal 

early and postmenopausal late using the Staging 

Reproductive Aging in Women (STRAW).10 Exclusion 

criteria included: history of bone disease, metabolic 

and/or endocrine disorders including hyperthyroidism, 

hyperparathyroidism, diabetes mellitus, liver disease, 

renal disease, and medications known to affect bone 

metabolism (e.g., corticosteroids, anticonvulsants, and 

heparin sodium). None of the participants had a history 

of medications for the treatment of osteoporosis, such as 

active vitamin D11, bisphosphonates, selective estrogen 

receptor modulators (SERM), or calcium.  

Laboratory measurements 

Five milliliters of fasting peripheral blood were 

drawn, centrifuged and kept frozen in the -20o C freezer 

until assayed. Serum samples were evaluated for levels 

of E2, FSH, LH levels, calcium, phosphorus, and vitamin 

D by ELISA (Thermo Fisher Scientific, USA) method.  

Bone mineral density measurements  

The bone ultrasound Mini-Omni (Sunlight, 

Beammed, Israel) was used to assess BMD. The 

parameter of speed of sound (SOS) m/s is used for the 

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analysis.12 The SOS refers to the division of transmission 

time of the sound waves by the length of the body part 

studied. The forearm and tibia bone scans were 

performed with the patient on the imaging table using the 

protocols recommended by the manufacturer. 

Osteoporosis was defined according to the conventional 

World Health Organization (WHO) definition.3,13 

Data analysis  

The comparisons of scores between groups were 

performed using t-tests, and correlations were assessed 

with the Spearman rank order test, with Bonferonni 

correction. The data were analyzed using Statistical 

Package Statistical Software version 20.0 (SPSS Inc., 

Chicago, IL). Significance was set at p<0.05 and was 

two-sided. 

 

Results 

Participant Characteristics 

Two hundred sixty (n=260) participants aged 

50.1±4.4 years were enrolled in the study. The average 

BMI was 27.3±5.2 kg/m2 and mean age of menopause 

was 48.4±3.4 years.  

Factors associated with bone density status 

The age of menopause (p=0.002), breastfeeding 

time (p=0.041), and serum vitamin D (p=0.025) were 

significantly associated with osteoporotic status. 

However, there were no statistically significant 

differences of BMI, menarche age, serum calcium, serum 

phosphorus, and parathyroid hormone levels noted 

between the three groups. The result of hormone analysis 

showed serum estradiol levels were lower in the 

osteoporotic group than in the normal BMD group 

(normal: 18.3±13.1 pg/ml, osteoporotic: 15.8±10.7 

pg/ml). The FSH and LH levels were higher in the 

osteoporosis group than in the normal BMD group (FSH 

normal: 54.5±44.1 pg/ml, FSH osteoporosis: 81.3±34.2 

pg/ml, LH normal: 53.1±41.2, LH osteoporosis: 

75.1±26.1 pg/ml). Clinical and laboratory characteristics 

of the participants are listed in Table 1. 

 

Table 1. Demographic and laboratory characteristics of 

participants 

 

Correlation of reproductive hormones with menopausal 

status 

Serum estradiol levels were not significantly 

different across menopause stages. The FSH and LH 

levels were higher in the postmenopausal late stage than 

in the premenopausal stage (Table 2). The study found a 

weak statistical correlation between FSH and SOS from 

the ultrasound (r=-0.16, p<0.01). There was a significant 

negative correlation between SOS and BMI (r=-0.306, 

p<0.01). The SOS was significantly different in all four 

groups (p<0.05).  

 

Table 2. Levels of reproductive hormones (by STRAW) 

stratified by menopausal status 

 

Analysis of bone mineral density 

The average T score was -0.18±0.6 in the 

normal BMD group, 1.67±0.4 in the osteopenia group, 

and -3.18±0.6 in the osteoporosis group. The Z score was 

0.29±1.2 in normal patients, -1.64±1.3 in the osteopenia 

group, and -2.17±1.1 in osteoporosis patient group.  

T-score and speed of sound progressively 

decreased with with age (Figures 1 and 2).  The box plots 

of T and Z scores of the participants stratified by 

menopausal status are shown in Figures 3 and 4.  

 

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Figure 1. Correlation between age and bone mineral 

density 

 

Figure 2. Correlation between age and speed of sound 

 

Figure 3. Box plot of T scores stratified by menopausal 

status 

 

Figure 4. Box plot of Z scores stratified by menopausal 

status 

 

Discussion 

The menopausal period is a normal 

physiological process that is accompanied by various 

symptoms.8 The researchers identified that the average 

age of onset of the menopause is 48-52, and it is similar 

in women across various countries.14  Recently published 

study demonstrated that the average age of menopause 

onset among Mongolian women was 49.3±3.1, 48.6±1.7 

and 48.2±2.9 years in 2008, 2010, and 2011, 

respectively.15 Similarly, in our study, the mean age of 

menopause for our research participants was 48.4±3.4 

years.  

The current study showed that the rate of 

osteoporosis was 11.2% and osteopenia was 34.6%, rates 

that were similar to results of other Asian women from 

reports of WHO in 2008.16 Osteoporosis incidence was 

higher in women with advanced stages of menopause. In 

our study, FSH and LH levels significantly differed 

across menopause stages in that those who were post-

menopausal had higher levels compared to those who 

were pre- or peri-menopausal.  Both hormones, FSH and 

LH, showed weak negative correlations with BMD level, 

but not E2. The result was significant in FSH level and 

SOS (r=-0.16; p<0.01), which was similar to previous 

studies.17,18 This could indicate that low BMD in later 

stages of menopause is associated with serum FSH  rather 

than E2. The weak correlation may be due to our small 

sample size. Other limitations of the current study 

include: participants were only selected from city areas 

and rural areas were not sampled, and the BMD was only 

tested in forearm and tibia. Ideally, the most common 

fracture sites, such as hips and spine, should be tested in 

future studies.  

 This is one of the first studies in Mongolia to 

determine the correlation between the hormonal levels 

and menopausal status. We concluded that women from 

older age groups had lower levels of serum estradiol, 

which were associated with loss of BMD. However, there 

was significant correlation between FSH and BMD in 

more advanced stages of menopause. Further study is 

needed to investigate the bone metabolism related studies 

to establish better epidemiological data sources among 

Mongolian population. Authors would like to encourage 

similar studies in Mongolia and Central Asia, consistent 

with the need of Cental Asian Region for better-

developed chronic disease research.19  

 

Conflict of Interest 

The author declares that they have no competing 

interests. 

 

Acknowledgement 

We wish to thank you all volunteers and the 

consultant gynecologist and the staff of the First 

Maternity Hospital.  

 

References 

1. Darba J, Kaskens L, Perez-Alvarez N, Palacios S, Neyro JL, 

Rejas J. Disability-adjusted-life-years losses in postmenopausal 

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women with osteoporosis: a burden of illness study. BMC Public 

Health. 2015;15:324. 

2. Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, 

Reginster JY. European guidance for the diagnosis and 

management of osteoporosis in postmenopausal women. 

Osteoporos Int. 2013;24(1):23-57. 

3. WHO. Assessment of osteoporosis at primary health care 

level. Summary Meeting Report 2004; 

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4. McKiernan FE, Berg RL, Linneman JG. The utility of BMD 

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osteoporosis. Osteoporos Int. 2011;22(4):1069-1077. 

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Khaltaev N. The diagnosis of osteoporosis. J Bone Miner Res. 

1994;9(8):1137-1141. 

6. Moon R, Cooper, C, Harvey, NC. Osteoporosis: 

Pathophysiology and Epidemiology. The Duration and Safety of 

Osteoporosis Treatment: Springer International Publishing; 

2016:1-16. 

7. Keating NL, Cleary PD, Rossi AS, Zaslavsky AM, Ayanian 

JZ. Use of hormone replacement therapy by postmenopausal 

women in the United States. Ann Intern Med. 1999;130(7):545-

553. 

8. Cauley JA, Seeley DG, Ensrud K, Ettinger B, Black D, 

Cummings SR. Estrogen replacement therapy and fractures in 

older women. Study of Osteoporotic Fractures Research Group. 

Ann Intern Med. 1995;122(1):9-16. 

9. Boroňová I BJ, Kľoc J, Tomková Z, Petrejčíková E, 

Mačeková S, Blaščáková MM. Analysis of OPG Gene 

Polymorphism T245G (rs3134069) in Slovak Postmenopausal 

Women. Analysis. 2014;2(12859). 

10. Soules MR, Sherman S, Parrott E, et al. Stages of 

Reproductive Aging Workshop (STRAW). J Womens Health Gend 

Based Med. 2001;10(9):843-848. 

11. Heinemann DF. Osteoporosis. An overview of the National 

Osteoporosis Foundation clinical practice guide. Geriatrics. 

2000;55(5):31-36; quiz 39. 

12. Chin KY, Ima-Nirwana S. Calcaneal quantitative 

ultrasound as a determinant of bone health status: what 

properties of bone does it reflect? Int J Med Sci. 

2013;10(12):1778-1783. 

13. WHO. Prevention and management of osteoporosis. 

Report of a WHO Scientific Group. . Geneva: World Health 

Organization;2003. 

14. Palacios S, Henderson VW, Siseles N, Tan D, Villaseca P. 

Age of menopause and impact of climacteric symptoms by 

geographical region. Climacteric. 2010;13(5):419-428. 

15. Ulziinorov G. The Relationship between Menopause 

Symptoms and the Quality of life of Women in Ulaabaatar City, 

Mongolia. Mahidol University: Institute for Population and Social 

Research;2009. 

16. Mithal A, Kaur P. Osteoporosis in Asia: a call to action. 

Curr Osteoporos Rep. 2012;10(4):245-247. 

17. Wu X YS, Zhang H, Xie H, Luo X, Peng Y, Liao E, et al. 

Early bone mineral density decrease is associated with FSH and 

LH, not estrogen. Clinica Chimica Acta. 2013;415:69-73. 

18. Xu  Z WA, Wu  X, Zhang H, Sheng Z, Wu X, Liao E. 

Relationship of age-related concentrations of serum FSH and LH 

with bone mineral density, prevalence of osteoporosis in native 

Chinese women. Clinica Chimica Acta. 2009;400(1-2):8-13. 

19. Adambekov S, Kaiyrlykyzy A, Igissinov N, Linkov F. Health 

challenges in Kazakhstan and Central Asia. J Epidemiol 

Community Health. 2016;70(1):104-108. 

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Table 1. Demographic and laboratory characteristics of participants 

Characteristics  Osteoporosis 

N=30 

Osteopenia 

N=90 

Normal 

N=140 

p-value 

Mean age 54.0±3.9 51.5±4.3 48.5±3.8 0.433 

BMI (kg/m2) 28.98±4.0 27.97±5.3 26.55±5.2 0.460 

Age at Menopause (years) 48.6±3.6 48.2 ±3.5 48.5±3.2 0.002 

Age at menarche (years) 14.72±1.8 14.47±1.7 14.98±1.9 0.464 

Number of birth (n) 3.3±1.5 3.2 ±1.5 2.6±1.2 0.167 

Serum calcium (mmol/l) 2.17±0.3 2.18 ±0.2 2.14±0.2 0.077 

Serum phosphorus (mmol/l) 3.63±0.9 3.76 ±1.0 3.55±0.9 0.261 

Serum PTH (pg/ml) 7.91±4.5 7.62 ±4.2 7.61±5.6 0.565 

Serum VitD (mmol/l) 13.28±6.1 12.52 ±4.9 12.58±6.1 0.025 

Breastfeeding time (yrs) 2.06±1.2 2.43±1.6 2.38±1.6 0.041 

 *Significant findings are indicated in bold.  

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Table 2. Levels of reproductive hormones (by STRAW) stratified by menopausal status  

Stage of menopause Premenopausal Perimenopausal Postmenopausal early Postmenopausal late 

 N=63 N=77 N=79 N=41 

Estradiol (pg/ml) 29.9±3.1  30.7±4.7  34.0±1.7  26.3±7.7 

FSH (pg/ml) 26.7±4.7 36.9±4.2 64.6±4.9  61.0±6.3 

LH (pg/ml) 20.5±3.6 34.4±3.5 62.3±4.7 59.7±6.9 

 

  

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Figure 1. Correlation between age and bone mineral density 

 

 

  

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Figure 2. Correlation between age and speed of sound 

 

  

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Figure 3. Box plots of T scores stratified by menopausal status 

 

  

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Figure 4. Box plots of Z scores stratified by menopausal status 

 

 

 

 

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