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Association between vasomotor symptoms and sarcopenia assessed by L3 skeletal muscle index among Korean menopausal women

Ryu, Ki-Jin MD; Kim, Hyun Kyun MD; Lee, Yeon Ju MD; Park, Hyuntae MD, PhD; Kim, Tak MD, PhD

Author Information
doi: 10.1097/GME.0000000000001879

Abstract

Sarcopenia is a disorder of age-related loss of muscle mass and function, which might be the most dramatic and significant change that occurs during the aging process.1 The importance of sarcopenia and age-related muscle changes has attracted considerable attention due to the aging of the population in most developed countries. Older women with sarcopenia are at increased risk of reduced mobility, diminished quality of life, cardiovascular risks, and fall-related injuries, which can lead to hip fractures and mortality.1-3 The prevalence of sarcopenia is rising worldwide and is reportedly 1%-24% among older Korean women.4,5 Postmenopausal women are at a particularly increased risk of sarcopenia, likely due to both aging and sex hormone changes after menopause, although the exact mechanisms underlying these associations remain unclear.6 In addition to aging and menopause, a sedentary lifestyle, reduced protein intake, changes in growth hormone levels, and increased inflammation have been suggested as risk factors for sarcopenia.7 Considering the high social burden caused by this disease, increased efforts should be made to elucidate the factors associated with sarcopenia and to perform early screening in at risk populations.

Unlike the well-described relationship between sarcopenia and menopause, the relationship between sarcopenia and variable menopausal symptoms has not yet been elucidated, although both are known to be affected by sex hormone changes.8 Vasomotor symptoms (VMS), including hot flashes and sweating, are among the most frequent and troublesome menopausal symptoms and affect approximately half of all Korean postmenopausal women.9 VMS are associated with several chronic disorders, including obesity, insulin resistance, metabolic syndrome, osteoporosis, and cardiovascular diseases.10 Several epidemiologic studies have reported an association between VMS and obesity assessed using body mass index (BMI) and waist circumference.11 However, such anthropometric measures are limited because they do not reflect the exact body composition, such as the percentage of adipose tissue versus muscle tissue. Because aging and menopause seem to be accompanied by diverse changes in the distribution of fat and muscle rather than equiproportional changes, it appears necessary to elucidate the association between VMS and body composition, including muscle mass.

Therefore, in the current study, we investigated the association between menopausal symptoms, including VMS and body composition indices measured by abdominal computed tomography (CT), and the prevalence of sarcopenia among otherwise healthy Korean menopausal women.

METHODS

Participants

This cross-sectional study included 314 South Korean postmenopausal women aged 40-65 years who self-referred for a routine health check at Korea University Anam Hospital (Seoul, South Korea) and underwent abdominal CT during their health check between January 2014 and May 2016. Several health check-up packages were available, including variable examinations, which they were free to choose with a range of costs. Abdominal CT was included in one such package, and it could also be added to any package at the participant's request. Therefore, the decision to undergo CT was completely dependent on the participant rather than the healthcare worker's advice. Postmenopausal status was defined as at least 12 consecutive months of amenorrhea without other medical causes. All women were interviewed and examined by an attending gynecologist. Written informed consent was obtained from all participants. This study was approved by the Institutional Review Board of the Korea University Medical Center (No. 2020AN0221).

Women were excluded from this study for the following reasons: lack of information on menopausal symptoms; current hormone use or use of any other drugs for the relief of VMS; current medication for diabetes mellitus or dyslipidemia; depressive mood disorder; overt thyroid disorder; history of hysterectomy or bilateral oophorectomy; history of chemotherapy or pelvic radiotherapy due to malignancy; presence of cardiovascular disease, such as prior myocardial infarction, angina, stroke, and peripheral arterial diseases; and chronic diseases, such as renal failure, liver cirrhosis, and current infectious diseases. Thus, a total of 295 women were included in this study.

Anthropometric and laboratory measurements

Height and weight were measured for each woman using a standard protocol, and BMI (kg/m2) was calculated using these results. Waist circumference was defined as the minimum circumference around the torso between the costal margin and the iliac crest, whereas the participants were standing upright and breathing normally. Each waist circumference measurement was repeated twice; if the measurements were within 1 cm of one another, the average was calculated. If the difference between the two measurements exceeded 1 cm, the two measurements were repeated until it no longer exceeded 1 cm. Overweight/obesity was defined as BMI ≥ 25.0 kg/m2. Blood pressure (BP) was measured using a standard mercury sphygmomanometer after the participants were at rest for at least 10 minute.

Laboratory data were collected from all women by venous blood sampling at 9:00 am after overnight fasting. Insulin levels were determined by radioimmunoassay using a commercially available kit (Biosource Europe S.A., Nivelles, Belgium). The homeostasis model assessment of insulin resistance index was calculated using the following formula: fasting plasma glucose (mg/dL) × fasting plasma insulin (IU/mL)/405. Measurements of fasting glucose, total cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, and triglycerides were assessed via routine clinical chemistry assessments.

Assessment of vasomotor symptoms

To assess VMS in menopausal women, we used a questionnaire based on the Menopause Rating Scale (MRS) that was developed and validated to measure the severity of menopause-related complaints.12 Each of the 11 questions included in the questionnaire was rated from 0 (no complaints) to 4 (extremely severe symptoms), depending on the perceived severity. From the first MRS results, a dichotomous variable was created for no VMS (MRS score of 0) or presence of VMS (MRS score of 1-4).

Assessment of body composition and diagnosis of sarcopenia

Plane imaging of the nonenhanced phase CT at the level of the transverse process of the third lumbar spine (L3) was analyzed using Aquarius iNtuition (TeraRecon, Foster City, CA, USA) by two investigators who were blinded to the study protocol and participants’ clinical data. The skeletal muscles were kept separate from other tissues by the validated Hounsfield unit (HU) threshold range of −29 to 150.13 Manual segmentation based on the HU thresholds was performed for skeletal muscle groups, and a segmentation algorithm automatically determined the visceral and subcutaneous fat areas; therefore, the cross-sectional areas of the paraspinal muscle area, bilateral psoas muscle area, rectus abdominis muscle area, oblique and transverse abdominis muscle, subcutaneous and visceral adipose tissue areas were identified (Supplemental Fig. 1, https://links.lww.com/MENO/A831). In the preliminary analysis to assess the interobserver variability in skeletal muscle area measurements with the CT images from 10 randomly selected women, the mean difference between the two investigators was only 0.14 cm2 (95% CI, −0.24 to 0.62). The skeletal muscle index (SMI) was defined by normalizing each skeletal muscle area (cm2) to the square of the participant's height (m2). We adopted the SMI cut-off for the diagnosis of sarcopenia that was introduced by Zhuang et al14 and is commonly used in Asian countries: SMI < 34.9 cm2/m2 in women.15

Other definitions

Information on the history of hormone therapy, current hormone use, alcohol intake, physical exercise level, and smoking history were obtained using a questionnaire. Current hormone use was defined as the use of sex steroid hormone replacement or use of oral contraceptives at the time of the visit. Alcohol intake was categorized according to the frequency of alcohol use per week as follows: none, 1 to 4 times per month, and more than once per week. Physical exercise was categorized according to the frequency of an activity lasting at least 20 minutes per day: none or once per week, 2 to 3 times per week, and more than 3 times per week.

Statistical analyses

The participants’ baseline characteristics, laboratory results, and severity of menopausal symptoms among the groups under study were compared using Student t test for continuous variables and Pearson χ2 test for categorical variables. Backward stepwise multivariate logistic regression analyses were performed to identify the association between sarcopenia and the odds of VMS. Due to the small number of participants, these analyses were performed in step-by-step increments of the number of independent variables. To accommodate the effect of covariates, Model 1 was adjusted for age, which was regarded to have a definite effect on both sarcopenia and VMS. Model 2 was adjusted for additional confounding factors, including BMI, waist circumference, visceral adipose tissue area, subcutaneous adipose tissue area, history of hormone therapy, systolic BP, diastolic BP, total cholesterol, homeostasis model assessment of insulin resistance index, alcohol intake, and physical exercise level. In addition, Model 3 was additionally adjusted for paraspinal muscle index, psoas muscle index, rectus abdominis muscle index, and oblique and transverse abdominis muscle index. However, the prevalence of sarcopenia was excluded from the covariates of Model 3, considering the possibility of collinearity with skeletal muscle indexes. Statistical significance was defined as a two-sided P value of < 0.05. All statistical analyses were performed using SPSS Statistics software (version 20.0; IBM Corp., Armonk, NY, USA).

RESULTS

The mean age of the study participants was 54.93 ± 6.20 years. A total of 135 women (45.8%) reported the absence of VMS, whereas 160 women (54.2%) reported any degree of VMS (86 mild, 48 moderate, 18 severe, and 8 very severe). Using the L3 SMI measured by abdominal CT, sarcopenia was diagnosed in 36 women (12.2%). The results of the comparisons of baseline characteristics, laboratory findings, abdominal CT, and dual-energy x-ray absorptiometry findings in the presence or absence of VMS are presented in Table 1. The SMI, paraspinal muscle index, and muscle/fat ratio were significantly higher in women with VMS than in those without. Furthermore, the prevalence of sarcopenia was more than double in women without VMS compared to that in women with VMS. The prevalence of sarcopenia was not significantly associated with the other 10 MRS items (Fig. 1).

TABLE 1 - Comparison of baseline characteristics, laboratory findings, and body composition indices measured with abdominal computed tomography by vasomotor symptoms among Korean menopausal women (n = 295)
Women without VMS (n = 135) Women with VMS (n = 160) P value
Age (y) 54.56 ± 7.06 55.24 ± 5.37 0.363
BMI (kg/m2) 22.98 ± 3.13 23.42 ± 3.30 0.239
Waist circumference (cm) 78.49 ± 8.31 78.76 ± 8.84 0.785
Obesity (BMI ≥ 25 kg/m2), % 22.4 27.5 0.314
History of hormone replacement therapy (%) 17.8 20.6 0.537
Alcohol (%) 0.238
 1-4 times per week 31.9 23.1
 ≥2 times per week 8.1 10.0
Exercise (%) 0.247
 2-3 times per week 19.3 26.2
 ≥4 times per week 8.9 5.6
Systolic BP (mm Hg) 106.67 ± 14.40 107.70 ± 13.45 0.525
Diastolic BP (mm Hg) 66.92 ± 9.67 67.69 ± 10.04 0.502
Fasting glucose (mg/dL) 94.76 ± 17.50 95.43 ± 15.15 0.728
HbA1c 5.67 ± 0.85 5.66 ± 0.43 0.918
HOMA-IR 1.94 ± 1.09 1.92 ± 1.15 0.859
TC (mg/dL) 191.27 ± 36.10 196.17 ± 36.15 0.247
HDL-C (mg/dL) 53.77 ± 11.82 55.38 ± 14.20 0.290
LDL-C (mg/dL) 125.13 ± 31.03 123.95 ± 34.61 0.761
TG (mg/dL) 100.93 ± 45.76 110.59 ± 59.58 0.125
Sarcopenia (%) 18.5 6.9 0.002
Skeletal muscle index (cm2/m2) 39.56 ± 5.29 41.23 ± 5.15 0.006
Paraspinal muscle index (cm2/m2) 17.59 ± 2.53 18.45 ± 2.39 0.003
Psoas muscle index (cm2/m2) 4.71 ± 1.04 4.83 ± 1.12 0.324
Rectus abdominis muscle index (cm2/m2) 3.30 ± 0.81 3.47 ± 0.95 0.113
Oblique and transverse abdominis muscle index (cm2/m2) 13.94 ± 2.50 14.42 ± 2.57 0.109
Visceral adipose tissue area (cm2) 82.32 ± 46.54 85.29 ± 44.62 0.578
Subcutaneous adipose tissue area (cm2) 155.70 ± 54.38 159.99 ± 63.53 0.538
Muscle/fat ratio 0.70 ± 0.10 0.72 ± 0.10 0.037
Data are expressed as means ± SDs unless otherwise specified.Statistical comparisons were conducted using Student t test for continuous variables and Pearson χ2 test for categorical variables.BMD, bone mineral density; BMI, body mass index; BP, blood pressure; HbA1c, glycated hemoglobin; HDL-C, high-density lipoprotein cholesterol; HOMA-IR, homeostasis model assessment of insulin resistance; LDL-C, low-density lipoprotein cholesterol; MRS, Menopause Rating Scale; TC, total cholesterol; TG, triglycerides; VMS, vasomotor symptoms.

FIG. 1
FIG. 1:
Comparison of the prevalence of menopausal symptoms included in the MRS by the presence or absence of sarcopenia among Korean menopausal women. MRS, Menopause Rating Scale. MRS 1: Vasomotor symptoms, MRS 2: Heart discomfort, MRS 3: Sleeping problems, MRS 4: Depressive mood, MRS 5: Irritability, MRS 6: Anxiety, MRS 7: Physical and mental exhaustion, MRS 8: Sexual problems, MRS 9: Bladder problems, MRS 10: Vaginal dryness, and MRS 11: Joint and muscular complaints. P value < 0.05 (statistical comparisons were conducted using the Pearson χ2 test).

The results of multivariate logistic regression analyses for the odds of the presence of VMS are presented in Table 2. Results showed that sarcopenia was inversely associated with the prevalence of VMS after adjusting for age (odds ratio [OR], 0.327; 95% CI, 0.15-0.69), and it was the only significant factor associated with VMS among several variables included in the Model 2 multivariate analysis (OR, 0.315; 95% CI, 0.15-0.67). When the four muscle indexes were included as covariates in the analyses instead of the prevalence of sarcopenia (Model 3), the paraspinal muscle index was positively associated with the prevalence of VMS (OR, 1.154; 95% CI, 1.04-1.27), and it was also only a significantly associated factor for VMS after adjusting for the same confounding factors included in the Model 2 analysis.

TABLE 2 - Multivariate logistic regression analysis of the odds of vasomotor symptoms among Korean postmenopausal women
OR for having VMS
Variable(s) a OR (95% CI) P value
Model 1 Sarcopenia b 0.327 (0.15-0.69) 0.004
Model 2 Sarcopenia b 0.315 (0.15-0.67) 0.003
Model 3 Paraspinal muscle index 1.154 (1.04-1.27) 0.005
Model 1 includes sarcopenia and age.Model 2 includes sarcopenia, age, BMI, waist circumference, history of hormone replacement therapy, systolic blood pressure, diastolic blood pressure, total cholesterol, HOMA-IR, alcohol intake (≥2 times per week), current smoking, physical exercise level, subcutaneous adipose tissue area, and visceral adipose tissue area.Model 3 includes paraspinal muscle index, psoas muscle index, rectus abdominis muscle index, oblique and transverse abdominis muscle index, age, BMI, waist circumference, history of hormone replacement therapy, systolic blood pressure, diastolic blood pressure, total cholesterol, HOMA-IR, alcohol intake (≥2 times per week), current smoking, physical exercise level, subcutaneous adipose tissue area, and visceral adipose tissue area.BMI, body mass index; CI, confidence interval; HOMA-IR, homeostasis model assessment of insulin resistance; OR, odds ratio; VMS, vasomotor symptoms.
aOnly statistically significant results are presented.
bWomen without sarcopenia were used as the reference group.

DISCUSSION

This study showed that, among the participants, less than half of postmenopausal women with sarcopenia experienced VMS compared to women without sarcopenia. The prevalence of sarcopenia in this study, assessed using L3 SMI measured by abdominal CT, was comparable to that reported in a recent review comparing the results from variable diagnostic methodologies.16 Furthermore, our results showed that the prevalence of VMS was positively associated with skeletal muscle mass, particularly the paraspinal muscle, independent of important confounding factors, including age, BMI, waist circumference, amount of adipose tissue, insulin resistance, and several lifestyle factors.

Only a few studies have attempted to investigate the association between menopausal symptoms and sarcopenia. A previous study conducted in Korea reported that lower handgrip strength, one of the most widely used physical performance measurements for the diagnosis of sarcopenia, was associated with a high Kupperman index score; however, none of the menopausal symptoms, including VMS, was assessed individually.17 Another study using data on handgrip strength, calf circumference, and gait speed reported that sarcopenia was associated with age, menopause, ethnicity, history of hysterectomy, mood disorders, joint/muscular discomfort, and VMS.18 To the best of our knowledge, this is the first study to reveal the association between VMS and sarcopenia assessed by skeletal muscle mass measured by abdominal CT. CT and readily available software for image analysis have made it possible to accurately assess skeletal muscle and fat, and CT-assessed sarcopenia has been investigated, particularly among cancer survivors.15 However, considering the various existing methodologies and definitions of sarcopenia, further longitudinal studies with comprehensive and validated diagnoses of sarcopenia are needed to confirm our findings.19

It is noteworthy that skeletal muscle mass was independently associated with VMS in this study because most of the previous studies reporting the association between VMS and being overweight/obese have assessed anthropometric measures, such as BMI, which are limited in assessing body composition.20 The paraspinal muscles, an intermediate layer of the intrinsic back muscles, run lengthwise along the spinal column and are associated with low back pain.21 We cannot explain exactly why the paraspinal muscle index was independently associated with VMS in this study. Although some authors have suggested that subcutaneous adipose tissue has an insulating effect and induces malfunction in response to core temperature changes,22 it is unknown whether trunk muscle masses may affect the core temperature and VMS severity. Furthermore, considering the recent studies showing increased fatty infiltration in the paraspinal muscles in women with low back pain,21 future studies in this field may need to assess intramuscular adipose tissue content along with muscle mass.

Recent studies with dual energy x-ray absorptiometry or quantitative CT have suggested an interrelationship between sarcopenia and osteoporosis.23 In addition to a similar population in which they occur, these conditions seem to be influenced by the same factors, such as growth hormone, vitamin D, and physical exercise.23 However, several studies have reported that VMS were associated with the risk of osteoporosis in menopausal women,10 in contrast to the negative relationship between VMS and sarcopenia observed in this study. Such discrepancies imply that complex physiologic mechanisms are involved in the relationships between VMS, and muscle and bone health, which should be determined by a further study.

Several studies have indicated that estrogen-based hormone therapy increases or preserves muscle strength in menopausal women.24 A recent meta-analysis found that hormone therapy was not associated with muscle mass.25 However, in a recent double-blinded randomized trial, testosterone treatment was associated with increased trunk muscle mass in women.26 Considering that a higher ratio of androgens to estrogens has been reportedly associated with VMS in middle-aged women,27 we hypothesize that androgen levels or the androgen-to-estrogen ratio may play a role in the association between VMS and muscle mass changes; however, we were unable to confirm this because of the lack of laboratory data on sex hormone levels in this study. Therefore, further studies are warranted to confirm the role of hormone therapy in preserving muscle mass, even in women without VMS.

There are some limitations in our study. First, the cross-sectional design of our study permitted the identification of associations, not causal relationships. Second, this study used the muscle mass index alone for the diagnosis of sarcopenia, although recent guidelines recommend considering skeletal muscle mass and strength together with a definitive clinical diagnosis.28 However, single-slice CT analysis is one of the most accurate methods for assessing body composition, including muscle mass. CT-assessed sarcopenia is a clinically valuable parameter that has been validated by several studies.15 Third, the odds ratio observed in this study may not be large; however, given the high prevalence of VMS and sarcopenia among postmenopausal women, such differences should still be regarded as significant. Fourth, VMS data were gathered by self-reporting MRS, which might be a subjective measurement, although the MRS questionnaire has been validated and used in many previous investigations.12 However, we dichotomized the scale of VMS into none and the presence of symptoms to reduce individual subjectivity on the description of the relative severity of symptoms. Fifth, although many confounding factors were assessed and statistically controlled, the possibility of residual confounding cannot be ruled out. Finally, the clinical implications of our findings remain unclear. However, this novel finding of an association between VMS and muscle mass, rather than adiposity or BMI, should be further investigated and may outline the direction of future studies to investigate the physiology of VMS and its determinants, including obesity and body composition.

CONCLUSIONS

Our data provide the first evidence that VMS are independently associated with skeletal muscle mass measured by CT and occurs less frequently in CT-assessed women with sarcopenia than in healthy Korean menopausal women. Considering that VMS are some of the major reasons that middle-aged women visit hospitals, healthcare providers should consider that menopausal women without VMS also need to be screened carefully given the high risk of sarcopenia observed in this study. However, further longitudinal studies should be conducted to confirm the causal relationships between VMS, skeletal muscle indices, fat and muscle distribution, and sarcopenia, as well as the underlying mechanisms.

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Keywords:

Hot flashes; Menopause; Obesity; Sarcopenia; Skeletal muscle index; Vasomotor symptoms

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Copyright © 2021 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of The North American Menopause Society.