Association of Sarcopenic Obesity and Body Composition With Metabolically Unhealthy Overweight/Obese Phenotypes Among Iranian Women: A Cross-Sectional Study

Abstract

Objectives

Obesity is a major risk factor for metabolic syndrome, with its prevalence has increased over the past decade. Major changes in body composition with aging have a significant effect on many clinical outcomes. Sarcopenic obesity consists of both the presence of abnormal adipose tissue with a deficit of muscle mass.

Results

Of the 241 subjects in this study (average age 35.32 years), 176 (73.03%) were classified as MUO phenotype. Based on this study, the prevalence of sarcopenic obesity was 7.88%. We found that high fat-free mass was more strongly and significantly associated with MUO phenotype. Furthermore, we found that individuals with high fat-free mass and high skeletal muscle mass had a significantly low prevalence of MUO phenotype. A significant positive correlation between metabolic phenotypes and sarcopenic obesity was also observed after all potential covariates were adjusted for. These results of this study suggest that increased adiposity and decreased skeletal muscle mass are associated with unfavorable metabolic traits among overweight and obese Iranian women. SO was also found to be associated with a greater risk of developing MUO phenotype.

Introduction

Obesity is an abnormal accumulation of fat that affects health negatively [1] with its prevalence having doubled since 1980 in middle-aged and older adults [2]. Previous studies reported 16.5% of Iranian subjects older than 18 years [3] and 24.8% of women aged 30 years and above as obese [4]. Obese subjects have been reported to have heterogeneous phenotypes with different degrees of metabolic risk [5]. A sub-group of obese individuals without associated metabolic complications have been phenotypically described as metabolically healthy obese (MHO) individuals [6, 7]. On the other hand is the metabolically unhealthy obese (MUO) individuals characterized by obesity-related metabolic complications [8]. Previous studies have reported MHO phenotype to be associated with a healthy metabolic profile, characterized by a lower amount of visceral adipose tissue (VAT) and liver fat [9], favorable lipid profile, high insulin sensitivity, and low pro-inflammatory cytokine levels in plasma [9, 10] than MUO subjects.

Major changes associated with aging in body composition include a decline in both fat-free mass and muscle strength referred to as sarcopenia [11]; and, an increase in body fat and a decline in skeletal muscle referred to as sarcopenic obesity (SO) [12]. Numerous studies have reported a significantly higher risk of mortality [13] worse cardiovascular risk profiles including hyperglycemia, hypertension, dyslipidemia, insulin resistance, and lower cardiorespiratory fitness [14–16] in sarcopenic obese individuals compared to non-sarcopenic or non-obese subjects.

Previous reports indicate a 9.9% prevalence of SO among Tehranian overweight/obese women [17], while a 10.9% and a 7.2% prevalence of MUO and MHO phenotypes respectively in Iranian adult population [18]. The aim of this study therefore was to determine the association of sarcopenic obesity and body composition with metabolically unhealthy overweight/obese phenotypes among Iranian women.

Methods

Results

Discussion

This study was conducted among overweight and obese Iranian women between the ages of 18–50 years, with a BMI ≥ 25 kg/m². The metabolic risk was assessed according to Karelis criteria and subjects classified as either MHO or MUO. Of the 241 subjects, 73.03% were classified as MUO with 7.88% as SO. We found that individuals with high FFM and high SMM to have a significantly low risk of MUO phenotype. We also found a significant positive correlation between sarcopenic obesity and MUO phenotype after all potential covariates were controlled.

This study’s MUO phenotypes showed a significantly higher BFM, VFM, FFM, SMM, and FMI than the MHO group. Previous studies have found that MUO women had significantly higher BFM, VFM, and muscle mass than MHO women [21] and healthy obese people [29].

Despite the fact that some studies [6, 22, 23] have observed a non-significant difference in the measures of adiposity in “healthy” and “unhealthy” phenotypes, in line with other previous studies [7, 24], we observed a significant increase in BFM in the MUO phenotype even after all potential confounders were controlled for. BFM has been reported as an independent predictor of insulin resistance and dyslipidemia [25] among postmenopausal women. Higher BFM has also been reported as an increased risk factor for type 2 diabetes [26, 27], as well as increase metabolic risk and the risk of cardiovascular disease [28, 29] in both gender. Furthermore, researches have shown increasing BFM to be correlated with an increase in FBG, triglyceride, LDL, and total cholesterol, and a decrease in HDL cholesterol [30, 31].

There have also been conflicting results regarding SMM accumulation among the metabolic phenotypes. While in some studies no significant differences in SMM indices between metabolic phenotypes of either obese or non-obese postmenopausal women [23] were found, some studies have reported SMM to significantly increase in the MUO phenotype of postmenopausal women [8, 32], and significantly decrease in the metabolic non-obese phenotype of young women (5). Estrella et al., [33] among Hispanic/Latino women found higher SMM to be independently associated with a lower prevalence of the MHO phenotype. In our study, each increase of 1-SD in skeletal muscle mass was associated with a lower prevalence of the MUO phenotype. Our result is in line with the fourth and fifth Korean National Health and Nutrition Examination Survey which reported a protective association of muscle mass with metabolic syndrome [34]. Additionally, in a 7-year retrospective cohort study, Kim and colleagues [35] found that an increase in relative skeletal muscle mass over time has a potential preventive effect on developing metabolic syndrome, independently of baseline skeletal muscle mass and glycometabolic parameters. In a nationally representative sample of 4,449 US adults aged 50 years and older from the NHANES surveys, Li and associates [36] found that only participants with low muscle mass but without metabolic syndrome had a significantly increased risk of all-cause mortality.

After we adjusted for all potential confounders, each increase of 1-SD in sarcopenic obesity was observed to be associated with a higher prevalence of MUO phenotype in the current study. In line with previous epidemiological studies, reports have shown that the odds of metabolic syndrome was 6 to 8 times higher in postmenopausal Korean women, elderly Korean men and women, and adult Caucasian subjects with sarcopenic obesity (SO) compared to those without sarcopenic obesity [14, 37–39]. Furthermore, Kim et al., [40] reported an increased risk of metabolic syndrome in subjects with sarcopenic obesity. In their study, compared with normal subjects, they found that SO subjects had significantly higher values for a number of metabolic syndrome components. Furthermore, they found SO to be independently associated with metabolic syndrome among women after adjustment for age.

Conclusion

In conclusion, increased adiposity and decreased skeletal muscle mass was associated with unfavorable metabolic traits among overweight and obese Iranian women. SO was also found to be associated with a greater risk of developing MUO phenotype after controlling for potential confounders.

Limitations

The cross-sectional nature of this study does not permit the assessment of causality. Also, we used BIA in order to assess body composition but not dual X-ray absorptiometry which is considered the gold standard method. However, BIA is also a validated and reliable method for the measurement of body composition [41]. Furthermore, the result of the current study cannot be generalized since only females were included in the study.

Abbreviations

Declarations

Ethical approval

This study was approved by the ethics committee of Tehran University of Medical Sciences (TUMS) with the following identification IR.TUMS.VCR.REC.1398.692.

Consent for publication

Not applicable.

Availability of data and materials

Participants of this study did not agree for their data to be shared publicly, so supporting data is not available.

Competing interests

All authors declared that they have no competing interests

Funding

This study is funded by grants from the Tehran University of Medical Sciences (TUMS). (Grant ID: 97-03-161-41155).

Author’s contributions

ATJ wrote the article, AM and NR revised the article, FSH performed the statistical analyses, KhM had full access to all of the data in the study and took responsibility for the integrity and accuracy of the data. All authors read and approved the final manuscript.

Acknowledgments

The authors thank the study participants for their cooperation and assistance in physical examinations. This study was supported by TUMS.

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