Back to Journals » Diabetes, Metabolic Syndrome and Obesity » Volume 14

Correlation Between the Distribution of Abdominal, Pericardial and Subcutaneous Fat and Muscle and Age and Gender in a Middle-Aged and Elderly Population

Authors Ni X, Jiao L, Zhang Y, Xu J, Zhang Y, Zhang X, Du Y, Sun Z, Wang S

Received 30 December 2020

Accepted for publication 8 April 2021

Published 17 May 2021 Volume 2021:14 Pages 2201—2208

DOI https://doi.org/10.2147/DMSO.S299171

Checked for plagiarism Yes

Review by Single anonymous peer review

Peer reviewer comments 2

Editor who approved publication: Prof. Dr. Juei-Tang Cheng



Xuefeng Ni,1 Li Jiao,1 Ye Zhang,1 Jin Xu,2 Yunqing Zhang,2 Xiaona Zhang,2 Yao Du,2 Zhaoyong Sun,2 Shitian Wang2

1Department of Healthcare, Peking Union Medical College Hospital, Beijing, 100730, People’s Republic of China; 2Department of Radiology, Peking Union Medical College Hospital, Beijing, 100730, People’s Republic of China

Correspondence: Li Jiao
Department of Healthcare, Peking Union Medical College Hospital, No. 1 of Shuaifuyuan Street, Dongcheng District, Beijing, 100730, People’s Republic of China
Tel +86 10 69157229
Email [email protected]

Objective: The present study aimed to explore the relationships between the distribution of abdominal fat and muscle and age and gender in a middle-aged and elderly population.
Methods: The levels of abdominal (visceral and subcutaneous) fat, pericardial fat, and psoas major muscle were measured in subjects who had physical examinations at the Health and Medical Department of Peking Union Medical College Hospital from July 2019 to June 2020. The relationship between fat in different areas (ie, different types of fat) and the relationship between different types of fat and the psoas major muscle were investigated in the context of different genders and ages.
Results: The distribution of fat and muscle differed between males and females of the middle-aged and elderly study sample. Volumes of pericardial fat, total abdominal fat, and visceral fat were significantly lower in females than in males, and the area of the psoas major muscle was also significantly lower in females than in males. Levels of subcutaneous fat and total abdominal fat showed no significant correlation with age. The level of muscle showed a significant negative correlation with age.
Conclusion: 1) Within the middle-aged and elderly sample, male subjects had higher levels than females of all types of fat except for abdominal subcutaneous fat, and had higher levels of psoas muscle than females. 2) Pericardial fat increased with age, whereas levels of abdominal fat did not change significantly with age. 3) The area of psoas major muscle appears to be positively correlated with volumes of all types of fat: subjects with more fat tended to have higher levels of psoas major muscle.

Keywords: middle-aged and elderly, abdominal fat, pericardial fat, psoas major muscle, age, gender

Introduction

In recent years, obesity has become an increasingly prominent social and medical problem both in China and globally. Obesity is accurately described as the presence of unhealthily excessive fat, increasing the risk of disease and death.1 Simple commonly used assessment methods include body mass index (BMI) and waist circumference measurement; more accurate methods for assessing fat require the use of dual-energy X-ray absorptiometry (DXA), computerised tomography (CT), or magnetic resonance imaging (MRI). The accuracy of BMI and waist circumference in assessing fat volumes is poor,2 and the accuracy is further reduced as patient age increases. In addition, the value of body fat has better predictive validity than BMI for the risk of metabolic syndrome3 and cardiovascular diseases.4 Muscle loss increases the risk of fractures and falls5 and affects quality of life and the ability to perform day-to-day tasks,6 and the need for long-term care of those elderly people who have lost the ability to live independently is a heavy burden on society.7–9 Muscle loss is also correlated with heart disease,10 respiratory disease,11 and even mortality.12 Studies concerning the distribution of fat and muscle in the population are essential for the prevention and treatment of chronic diseases. However, there is a lack of studies focusing specifically on middle-aged and elderly patients, especially studies specific to abdominal (subcutaneous and visceral) fat, pericardial fat, and muscle. Therefore, the present study investigated the correlation between abdominal fat, pericardial fat, and muscle in middle-aged and elderly people of different genders and ages. With the widespread availability of CT scanners, as well as their advantages as simple, reliable, and non-invasive means of assessing the distribution of visceral fat and muscle, the CT examination is considered the current gold standard for measuring levels of fat and muscle. The properties of tissues can be judged by the CT values in combination with computer software to accurately calculate the levels of fat and muscle in the body.

Subjects and Methods

Study Subjects

The data of patient subjects undergoing physical examination at the Health and Medical Department of Peking Union Medical College Hospital from July 2019 to June 2020 were analyzed. Levels of psoas major muscle in the subjects were measured from September 2020.

The COVID-19 infection was excluded from all subjects undergoing physical examinations after 2020. Subjects with acute infections, new onset of severe trauma, surgical history, newly discovered tumors, and endocrine diseases that might cause significant changes in weight, such as hyperthyroidism, were excluded.

Methods

The present study was a retrospective cross-sectional study. The physical examination subjects were all covered by medical reimbursements. The general information of each examinee (including gender, age, height, body weight, waist circumference, and blood pressure) was collected and the BMI calculated. Waist circumference was measured from the plane of the anterior superior iliac crest at the end of expiration to the midpoint of the lower costal margin. BMI was calculated as body mass (kg)/body height (m). Thoracic, abdominal, and pelvic CT was conducted in all subjects, and measurements of abdominal fat and pericardial fat were taken for all subjects.

The CT scanner was the Siemens Definition Flash with CARE Dose 4D, with scanning condition 120 kV, scanning thickness 0.5 mm, and B30f reconstruction. In Figure 1, “pericardial fat” refers to the volume of fat (in cm3) within the pericardium on the CT image, with the inferior border of the heart as the lower edge and the aortic bifurcation as the upper edge. Measurement of abdominal fat (in cm3) was taken with the diaphragm as the upper edge of the abdominal border, and the upper edge of the iliac crest as the lower edge: all fat in this region was recorded as abdominal fat. The volume of abdominal visceral fat was measured (in cm3) as the volume of fat inside the peritoneum, and the volume of abdominal subcutaneous fat was measured (in cm3) as the volume of fat outside the peritoneum. The volume of pelvic visceral fat (in cm3) was the volume of all intra-peritoneal fat from the upper edge of the iliac crest to the lower edge of the pelvic floor. The psoas major muscle was measured at the level of the lumbar 3 intervertebral disc, and the area of the psoas major muscle was taken as the sum of the bilateral psoas major muscle area (in cm2).

Figure 1 Schematic diagram of the measurement of abdominal fat. (A) Sagittal CT of the chest and abdomen. The marked area indicates abdominal fat (including subcutaneous fat and visceral fat), the yellow area indicates pelvic visceral fat, and the area around the heart is pericardial fat. (B) Coronal CT of the chest and abdomen. The marked area indicates abdominal fat (including subcutaneous fat and visceral fat), the yellow area indicates pelvic visceral fat, and the area around the heart is pericardial fat.

Statistic Processing

All research data were recorded using EXCEL 2010, and data was analyzed using SPSS 24.0. Age, body weight, height, waist circumference, BMI, volume of abdominal visceral fat, volume of abdominal subcutaneous fat, total abdominal fat, percentage of abdominal visceral fat, volume of pericardial fat, and area of psoas muscle were all expressed by x ± s. A two-tailed t-test was used for numerical comparison between groups. P < 0.05 was considered statistically significant.

Results

Distribution of the General Characteristics of the Patients Undergoing Physical Examinations (Tables 1 and 2)

In those aged 50–100 years in the population who underwent physical examination, a total of 471 patients underwent CT examinations of the chest, abdomen, and pelvis, including 409 males and 62 females. Testing indicated that the distribution of the data concerning fat and muscle in each group conformed to normal distribution.

Table 1 The General Characteristics of the Patients

Table 2 Clinical Data of the Patients

Levels of Fat and Muscle in Middle-Aged and Elderly People of Different Genders (Table 3)

In the population aged over 50 years, males and females had different distributions of fat and muscle. Females had significantly less pericardial fat and significantly less abdominal visceral fat than males, thus females had significantly less visceral fat than males. The level of total abdominal fat in females was significantly less than that in males. There was no significant difference between females and males in terms of volumes of abdominal subcutaneous fat.

Table 3 Fat and Muscle Levels in Middle-Aged and Elderly People of Different Genders

Correlation of Age with Levels of Fat and Muscle (Table 4)

Levels of subcutaneous fat and total fat had no significant correlation with age. The level of muscle showed a significant negative correlation with age.

Table 4 The Correlation Between Age and Fat of Different Parts and Psoas Major Muscle

Correlation of Pericardial Fat with Abdominal Fat (Table 5)

For subjects aged over 50 years, there existed significant correlation between volume of pericardial fat and volume of other types of fat, BMI, and waist circumference; of these, the correlation between levels of pericardial fat and visceral fat and waist circumference was most obvious.

Table 5 The Correlation Between the Pericardial Fat and Abdominal Fat and Psoas Major Muscle

Correlation Between Area of Psoas Major Muscle and Volume of Abdominal Fat (Table 4)

For those aged over 50 years, the area of the psoas major muscle was correlated with the volume of abdominal fat.

Discussion

It is generally believed that obesity is a risk factor for all-cause mortality regardless of the presence of common metabolic abnormalities.13 Studies in the last century confirm that central obesity is associated with the risk of diabetes mellitus,14,15 cardiovascular disease and events,16,17 and hypertension.18 Since the beginning of this century, it has been discovered that obesity is related to overall risk of sleep apnea,19 cancer,20 and mortality.21 Mortality in males and females with waist circumference in the highest 20% of the population is almost twice that in those with waist circumference in the lowest 20%. According to the fat volume measurement in the present study, total abdominal fat was lower in females than in males; this was especially the case for abdominal visceral fat.

Analysis of the US 1999–2006 National Health and Nutrition Examination Survey (NHANES) data shows that for a population with an average age of 46, BMI and body fat percentage were lower in males than in females, whereas waist circumference was higher in males than in females. That study included mainly white, Hispanic, and non-Hispanic black individuals.22 In the present study, all subjects were of East Asian “yellow races” and were relatively older, with an average age of 69; the population was characterized by relatively affluent living and medical conditions. Under these conditions, it was found that BMI and waist circumference were significantly higher in males than in females. Concerning fat distribution, with the exception of abdominal subcutaneous fat, the volume of which was similar in males and females, volumes of all other fat types (pericardial, abdominal visceral, and pelvic fat) were significantly higher in males; the area of muscle was also significantly higher in males than in females. Although the current mainstream view is that waist circumference should be evaluated separately in males and females, some papers claim that the same standard of waist circumference should be used for both genders.22

Adipocytes around the heart originate from the mesoderm and have the same embryonic origin as mesenteric and omental adipocytes.23 Under normal circumstances, pericardial fat accounts for approximately 20% of heart weight.24 Pericardial fat is concentrated mainly in the atrioventricular and ventricular grooves, so the coronary arteries and their main branches are usually buried in the pericardial fat. Data from the Framingham Heart Study published in 2008 shows that pericardial fat and obesity (measured by weight and waist circumference) were correlated with various indicators of risk factors in cardiovascular disease (hypertension, hypertriglyceridemia, low high-density lipoprotein cholesterolemia, impaired fasting blood glucose, and diabetes mellitus), and had a significant correlation with metabolic syndrome. The correlation with the metabolic risk factors still existed after adjustment for body weight and waist circumference, but there was no significant difference after adjustment for abdominal visceral fat level.25–27 Further studies have found that pericardial fat is an independent risk factor for coronary atherosclerosis, and that with every 10 cm3 increase in the volume of coronary fat, the probability of progression of coronary calcification score increases by 12%28. In the population with a coronary calcification score of 0, pericardial fat is also an important predictor for coronary non-calcified plaque.29

In the present study, males had significantly more pericardial fat than females. In terms of the relationships between pericardial fat and other fat types, the correlation between volumes of pericardial fat and abdominal visceral fat is the most obvious; the correlation between pericardial fat and abdominal subcutaneous fat is less clear. This may be because pericardial fat and abdominal visceral fat share a common origin. Unlike other fat types, which display no significant correlation with age, pericardial fat is in a statistically weak positive correlation with age. This might suggest a slow increase in volume of pericardial fat with age; further longitudinal studies are required to assess this.

Sarcopenia is an important manifestation of aging. The common signs of sarcopenia include decreased muscle strength, decreased muscle mass, and decreased physical function.30 Muscle volume can be measured by bioelectrical impedance analysis, DXA, CT, or MRI; muscle volume results as detected by CT and MRI are currently considered the benchmark. The horizontal area of the psoas major muscle can be easily measured by CT, and the psoas major index has been suggested as a possible value for assessing muscle volume throughout the body.31 To date, several studies have found a correlation between the level of psoas major muscle and arteriosclerosis and coronary heart disease in non-elderly individuals.32 In the middle-aged and elderly subjects enrolled in the present study, the area of psoas major muscle decreased with age, but was positively correlated with volumes of abdominal and pericardial fat. It is therefore suggested that the level of psoas major muscle might be significantly correlated with nutritional status in middle-aged and elderly individuals. The correlation was more obvious after adjusting for age. In recent years, sarcopenic obesity in the elderly has been a focal issue in geriatrics. However, the results of the present study suggest that where both sarcopenia and obesity exist, there would be a risk of further muscle loss if fat volume were reduced. Clinically, therefore, further research into the control of fat levels in the elderly is necessary. However, our limitation is that the majority of participants were males (87%) in the whole study, which may suggest a sex bias. And HDL and total cholesterol were higher among females than in males, but we did not assess the possible effects of these changes in lipid profiles on the correlation of fat depots.

Conclusion

Among the middle-aged and elderly study population, volumes of fat of all types, except for abdominal subcutaneous fat, were higher in males than in females, and males also had higher levels of the psoas major muscle than females. Pericardial fat volume increased with age while abdominal fat volume did not change significantly with age. The area of the psoas major muscle was positively correlated with the volume of each type of fat, ie, individuals with more fat tended to have higher levels of psoas major muscle.

Ethics Approval and Consent to Participate

This study was conducted in accordance with the declaration of Helsinki. This study was conducted with approval from the Ethics Committee of Peking Union Medical College Hospital. A written informed consent was obtained from all participants.

Consent for Publication

Consent for publication was obtained from every individual whose data are included in this manuscript.

Disclosure

All authors have contributed significantly to the manuscript and declare that the work is original. None of the authors have any financial disclosures or conflicts of interest.

References

1. Villareal DT, Apovian CM, Kushner RF, Klein S; American Society for Nutrition; NAASO, The Obesity Society. Obesity in older adults: technical review and position statement of the American Society for Nutrition and NAASO, The Obesity Society. Obes Res. 2005;13(11):1849–1863. doi:10.1038/oby.2005.228

2. Batsis JA, Mackenzie TA, Bartels SJ, Sahakyan KR, Somers VK, Lopez-Jimenez F. Diagnostic accuracy of body mass index to identify obesity in older adults: NHANES 1999–2004. Int J Obes (Lond). 2016;40(5):761–767. doi:10.1038/ijo.2015.243

3. Fox CS, Massaro JM, Hoffmann U, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007;116(1):39–48. doi:10.1161/CIRCULATIONAHA.106.675355

4. Després JP. Body fat distribution and risk of cardiovascular disease: an update. Circulation. 2012;126(10):1301–1313. doi:10.1161/CIRCULATIONAHA.111.067264

5. Schaap LA, van Schoor NM, Lips P, Visser M. Associations of sarcopenia definitions, and their components, with the incidence of recurrent falling and fractures: the longitudinal aging Study Amsterdam. J Gerontol a Biol Sci Med Sci. 2018;73(9):1199–1204. doi:10.1093/gerona/glx245

6. Beaudart C, Biver E, Reginster JY, et al. Validation of the SarQoL®, a specific health-related quality of life questionnaire for Sarcopenia. J Cachexia Sarcopenia Muscle. 2017;8(2):238–244. doi:10.1002/jcsm.12149

7. Mijnarends DM, Luiking YC, Halfens RJG, et al. Muscle, health and costs: a glance at their relationship. J Nutr Health Aging. 2018;22(7):766–773. doi:10.1007/s12603-018-1058-9

8. Dos Santos L, Cyrino ES, Antunes M, Santos DA, Sardinha LB. Sarcopenia and physical independence in older adults: the independent and synergic role of muscle mass and muscle function. J Cachexia Sarcopenia Muscle. 2017;8(2):245–250. doi:10.1002/jcsm.12160

9. Steffl M, Bohannon RW, Sontakova L, Tufano JJ, Shiells K, Holmerova I. Relationship between sarcopenia and physical activity in older people: a systematic review and meta-analysis. Clin Interv Aging. 2017;17(12):835–845. doi:10.2147/CIA.S132940

10. Bahat G, Ilhan B. Sarcopenia and the cardiometabolic syndrome: a narrative review. Eur Geriatr Med. 2016;6(3):220–223. doi:10.1016/j.eurger.2015.12.012

11. Bone AE, Hepgul N, Kon S, Maddocks M. Sarcopenia and frailty in chronic respiratory disease. Chron Respir Dis. 2017;14(1):85–99. doi:10.1177/1479972316679664

12. De Buyser SL, Petrovic M, Taes YE, et al. Validation of the FNIH sarcopenia criteria and SOF frailty index as predictors of long-term mortality in ambulatory older men. Age Ageing. 2016;45(5):602–608. doi:10.1093/ageing/afw071

13. Kuk JL, Ardern CI. Are metabolically normal but obese individuals at lower risk for all-cause mortality? Diabetes Care. 2009;32(12):2297–2299. doi:10.2337/dc09-0574

14. Bray GA, Jablonski KA, Fujimoto WY, et al. Diabetes prevention program research G relation of central adiposity and body mass index to the development of diabetes in the diabetes prevention program. Am J Clin Nutr. 2008;87(5):1212–1218. doi:10.1093/ajcn/87.5.1212

15. Goodpaster BH, Thaete FL, Simoneau JA, Kelley DE. Subcutaneous abdominal fat and thigh muscle composition predict insulin sensitivity independently of visceral fat. Diabetes. 1997;46(10):1579–1585. doi:10.2337/diacare.46.10.1579

16. Kannel WB, Cupples LA, Ramaswami R, Stokes J 3rd, Kreger BE, Higgins M. Regional obesity and risk of cardiovascular disease; the Framingham Study. J Clin Epidemiol. 1991;44(2):183–190. doi:10.1016/0895-4356(91)90265-B

17. Donahue RP, Abbott RD. Central obesity and coronary heart disease in men. Lancet. 1987;2(8569):1215. doi:10.1016/S0140-6736(87)91357-2

18. Cassano PA, Segal MR, Vokonas PS, Weiss ST. Body fat distribution, blood pressure, and hypertension. A prospective cohort study of men in the normative aging study. Ann Epidemiol. 1990;1(1):33–48. doi:10.1016/1047-2797(90)90017-M

19. Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Clin Endocrinol Metab. 2000;85(3):1151–1158. doi:10.1210/jcem.85.3.6484

20. Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol. 2013;62(10):921–925. doi:10.1016/j.jacc.2013.06.027

21. Pischon T, Boeing H, Hoffmann K, et al. General and abdominal adiposity and risk of death in Europe. N Engl J Med. 2008;359(20):2105–2120. doi:10.1056/NEJMoa0801891

22. Grundy SM, Williams C, Vega L. Upper body fat predicts metabolic syndrome similarly in men and women. Eur J Clin Invest. 2018;48(7):e12941. doi:10.1111/eci.12941

23. Ho E, Shimada Y. Formation of the epicardium studied with the scanning electron microscope. Dev Biol. 1978;66(2):579–585. doi:10.1016/0012-1606(78)90263-4

24. Corradi D, Maestri R, Callegari S, et al. The ventricular epicardial fat is related to the myocardial mass in normal, ischemic and hypertrophic hearts. Cardiovasc Pathol. 2004;13(6):313–316. doi:10.1016/j.carpath.2004.08.005

25. Rosito GA, Massaro JM, Hoffmann U, et al. Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study. Circulation. 2008;117(5):605–613. doi:10.1161/CIRCULATIONAHA.107.743062

26. Ding J, Kritchevsky SB, Harris TB, et al.; Multi-Ethnic Study of Atherosclerosis. The association of pericardial fat with calcified coronary plaque. Obesity (Silver Spring). 2008;16(8):1914–1919. doi:10.1038/oby.2008.278.

27. Iwasaki K, Matsumoto T, Aono H, Furukawa H, Samukawa M. Relationship between epicardial fat measured by 64-multidetector computed tomography and coronary artery disease. Clin Cardiol. 2011;34(3):166–171. doi:10.1002/clc.20840

28. Yerramasu A, Dey D, Venuraju S, et al. Increased volume of epicardial fat is an independent risk factor for accelerated progression of sub-clinical coronary atherosclerosis. Atherosclerosis. 2012;220(1):223–230. doi:10.1016/j.atherosclerosis.2011.09.041

29. Ito T, Suzuki Y, Ehara M, et al. Impact of epicardial fat volume on coronary artery disease in symptomatic patients with a zero calcium score. Int J Cardiol. 2013;167(6):2852–2858. doi:10.1016/j.ijcard.2012.07.026

30. Cruz-Jentoft AJ, Bahat G, Bauer J, et al.; Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16–31. doi:10.1093/ageing/afy169.

31. Hamaguchi Y, Kaido T, Okumura S, et al. Proposal for new diagnostic criteria for low skeletal muscle mass based on computed tomography imaging in Asian adults. Nutrition. 2016;32(11–12):1200–1205. doi:10.1016/j.nut.2016.04.003

32. Imaizumi T, Shiga Y, Idemoto Y, et al. Associations between the psoas major muscle index and the presence and severity of coronary artery disease. Medicine (Baltimore). 2020;99(28):e21086. doi:10.1097/MD.0000000000021086

Creative Commons License © 2021 The Author(s). This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution - Non Commercial (unported, v3.0) License. By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms.