A.J. Santanasto1, I. Miljkovic1, R.K. Cvejkus1, R.M. Boudreau1, V.W. Wheeler2, J.M. Zmuda1
1. Department, of Epidemiology, University of Pittsburgh, Pittsburgh, PA, USA; 2. Tobago Health Studies Office, Scarborough, Tobago, Trinidad & Tobago
Corresponding Author: Adam J. Santanasto, Department, of Epidemiology, University of Pittsburgh, Pittsburgh, PA, USA, firstname.lastname@example.org
J Frailty Aging 2021;in press
Published online December 2, 2021, http://dx.doi.org/10.14283/jfa.2021.47
Body composition and muscle strength change vary by age and ethnicity, and have a major impact on health and physical function. Little is known about the patterns of these changes in African-ancestry populations. Herein, we examined age-specific (5-year age groups) rates-of-change in lean and fat mass in 1918 African-ancestry men on the Caribbean island of Tobago (baseline age: 62.0±11.8 years, range: 40-99 years). Body composition (DXA) and grip strength were measured at three time points (baseline, 4- and 9-year follow-up). Annualized rates of change were calculated with all 3 time-points using Generalized Estimating Equations. We found that whole body lean mass declined at constant rate until age 65 (-0.72%/year; 95% CI: -0.76, -0.67), which accelerated to -0.92 %/year (-1.02, -0.82) among those 65-69, and again to -1.16 %/year (-1.30, -1.03 ) among those aged 70+. Whole body fat mass increased by a near constant rate of 2.93 %/year (2.72, 3.15%) across the lifespan. Finally, grip strength decline accelerated at age 50, and about 2x faster than lean mass through the lifespan after the age of 50. To conclude, in African-Caribbean men, the acceleration in muscle strength decline precedes the acceleration in lean mass decline by 10-15 years, suggesting decrements in factors other than lean mass drive this initial acceleration in muscle strength decline. We also found that African-Caribbean men undergo a constant shift to a more adipogenic phenotype throughout the adult lifespan (aged 40-99), which likely contributes to age-related loss of muscle and physical function.
Key words: African ancestry, body composition, muscle strength, longitudinal, epidemiology.
Body composition changes with aging vary by age, sex, and ethnicity and have a major influence on health, and physical function across the lifespan in older adults (1-3). When examined cross-sectionally, African Americans generally have higher whole body lean mass and muscle strength than similarly aged Caucasians (4). Similarly, we have recently shown that African Caribbean men have a relatively low prevalence of sarcopenia – defined as low lean mass and muscle strength (5). However, African American men and women tend to lose lean mass and muscle strength at faster rates than Caucasians (1). Little is known about body composition patterns across the lifespan of African ancestry individuals outside the U.S. Herein, we describe longitudinal changes in lean mass, fat mass, and grip strength over a 9-year period in a unique cohort of African Caribbean men aged 40-99 on the island of Tobago. The relationship between concurrent changes in body composition and grip strength was also examined.
Originally, 3170 men aged ≥40 years on the Caribbean island of Tobago participated in a prostate-specific antigen screening study (~60% of age eligible men on the island) (6). To participate, men had to be ambulatory, noninstitutionalized adults without terminal illness. Between 2004 – 2007 (baseline for the current analyses), all men were invited to have a dual x-ray absorptiometry (DXA) scan for the first time and 2667 men aged ≥40 years completed the visit. DXA measurements were repeated 6- and 9-years later and the analytic sample for these analyses included the 1918 men that had baseline, and at least one follow-up body composition and grip strength measurement. Of these, 1320 men had data at all 3 time points, 528 had baseline and 6-year data only, and 70 men had baseline and 9-year data only. Written informed consent was obtained from all study participants and the study was approved by the Institutional Review Boards of the University of Pittsburgh and the Tobago Division of Health and Social Services.
Anthropometry, Body Composition and Grip Strength Measures
Height (cm) was measured using a wall-mounted stadiometer and body weight (kg) was measured on a balance beam scale, without shoes. Height and weight were used to calculate body mass index (BMI, kg/m2).
Whole body DXA scans were conducted at baseline and both follow-up visits using the same QDR 4500W densitometer (Hologic, Inc.). Scans were analyzed for whole body soft-tissue (which excludes bone material) lean and fat mass, as well as appendicular lean mass using QDR software version 8.26a.
Grip strength was measured using a Jamar handheld dynamometer at each time point. At baseline and both follow-up visits, participants were instructed to stand with the elbow of the hand being tested tucked to their side, with the forearm extended. They then asked to squeeze the dynamometer as hard as they could. Each hand was tested two times. For baseline, the maximum grip strength from among the 4 tests was used in analyses. For follow-up, the maximum grip-strength of the hand that was used for baseline was used in analyses.
Information on lifestyle habits, demographic factors, medical conditions, and medication use was collected using interviewer-administered questionnaires. Hypertension was defined as presenting with a systolic blood pressure ≥140mmHg or diastolic blood pressure ≥90mm, or taking hypertension medication, or self-reported physician diagnoses. Diabetes was defined as self-reported treatment, or presenting with fasting blood glucose ≥126mmol/L. Cardiovascular disease (CVD) was defined as self-reported history of heart attack, stroke or congestive heart failure. Smoking was recorded as never (<100 cigarettes or 5 packs lifetime) or ever smoked (≥100 or 5 packs cigarettes lifetime). Alcohol consumption was categorized as: >1 drink/day or ≤1 drink/day. In order to assess walking for leisure or exercise, self-reported frequency of walking outside the home during the past week was asked. Participants were dichotomized into those who walked “often” (5-7 days per week) to those who walked “sometimes” or less (<5 days per week).
Means and standard deviations or frequencies and percents were calculated for all baseline demographic, descriptive and body composition measures. Annualized rates of change and 95% confidence intervals were calculated using all available time-points with Generalized Estimating Equations (GEE). Annualized percent change was based on two timepoint GEE repeated measures models based on percent change from baseline to 6-years and 9-years. Time was treated as linear to estimate average annualized change and percent change. An unstructured covariance was used in all models. These data were generated overall and stratified by 5-year age groups. Separate multivariable GEE models were also used to quantify the association between concurrent changes in body composition depots and grip strength. First, we examined these associations unadjusted (model 1), then adjusted for age, height, weight, and smoking status (model 2), and additionally adjusted for prevalent chronic diseases (model 3). To account for associations that vary over time, time interactions for all main effects and covariates were included in each model.
Baseline characteristics of the analytic sample are depicted in Table 1. Men were aged 62 ± 11.8 years (range: 40-99), had a BMI of 27.4 ± 4.3 kg/m2 and 26.7% completed high school or higher levels of education (Table 1).
We examined the annualized percent change in body composition depots, overall and stratified by 5-year baseline age groups (Table 2). Fat mass increased, whereas lean mass decreased over time – overall and in every age stratum. Whole body fat mass increase was fairly uniform (2.5 – 3.5% per year) across the lifespan, except in those 80+, where fat mass increase slowed to 1.5% per year. Appendicular fat mass increased at near identical rates to whole body fat mass across the lifespan. Whole body lean mass declined by a near constant rate (range: -0.63 – -0.78%/year) from age 45-64 yrs and accelerated to -0.92 %/year (95% CI: -1.02 – -0.82) among those 65-69, and again to -1.16 %/year (95% CI: -1.30 – -1.03 ) in those 70 year and older (Table 2). As with fat mass, appendicular lean mass declined at near identical rates to whole body lean mass.
*Changes were determined using GEE, and data are mean percent change per year (95% confidence intervals).
In all men combined, grip strength declined at a faster tempo compared with the decline in lean mass. Specifically, grip strength declined 3.4x faster per year than total lean mass, 1.9x faster per year than arm lean mass, 2.0x faster per year than leg lean mass and 1.9x fast per year than appendicular lean mass. The dissociation between change in grip strength and change in lean mass did not become evident until age 50, as grip strength only declined 1.3x faster per year than lean mass in those aged 40-49 years. After the age of 50, grip strength declined approximately 2x faster per year than lean mass (range: 1.61x – 2.67x faster per year) with the largest dissociation occurring in those aged 80 years and older (Table 2).
We next examined the associations between changes in regional body composition measures with concurrent changes in grip strength using separate GEE models (Table 3). When the associations were examined adjusted only for follow-up time (model 1), all 4 body composition measures were significantly, positively associated with changes in grip strength. The time interaction for both arm fat and appendicular fat were negative and significant, indicating the association between fat mass and grip strength weakened over time. When baseline body weight was included in the models (model 2), the betas for change in arm fat and appendicular fat flipped and these depots became significantly negatively associated with grip strength. After adjustment for baseline weight, changes in arm and appendicular lean mass remained significantly positively associated with change in grip strength. Adjustment for hypertension, diabetes, cardiovascular disease, stroke, cirrhosis, arthritis, and emphysema (model 3) had little effect on the associations between changes in lean and fat mass with changes in grip strength.
*Data are beta coefficients (SE) from separate GEE models per row; **Beta coefficients represent grip strength change per year (in kilograms), per 1-kilogram concurrent change in body composition.
In this study of African Caribbean men, we found that soft tissue lean mass decreases, whereas fat mass increases across the adult lifespan. These observations indicate that African Caribbean men undergo body composition remodeling across their lifespan, resulting in a more adipogenic phenotype with age. We also found that fat mass increased at a fairly constant rate from the fourth through the seventh decade of life and slowed thereafter. In contrast, lean mass declined at a constant rate through the sixth decade of life, and decline accelerated thereafter, especially in those 70 and older. We also found that grip strength weakened throughout the adult lifespan in African Caribbean men. Interestingly, the initial acceleration in grip strength decline occurred at age 50, 15 years prior to the initial acceleration in loss of lean mass. The second acceleration in appeared to occur at age 60, 10 years prior to the second acceleration in lean mass. Further, grip strength declined about two times faster than lean mass across the lifespan. This suggests that factors other than lean mass – such as neuromuscular junction health, intermuscular and intramyocellular lipids and fibrosis – may play a role in muscle strength decline in these men.
The fact that grip strength declined faster than lean mass corroborates findings in older African American and Caucasian men aged 70+ enrolled in the Health ABC Study (1). African American and Caucasian men in Health ABC lost 1.3% and 1.0% of their leg lean mass per year, respectively – which was nearly identical to the 1.1% annual loss of leg lean mass experienced by the African Caribbean men aged 70+ in the current study. However, African American and Caucasian men in Health ABC experienced a 4.1%/year and 3.4%/year decline in leg strength, respectively – whereas men in the current study only experienced a 2-3%/year decline in handgrip strength (1). The discrepancy between muscle strength loss in the current study compared with Health ABC may be due to differences in muscle strength assessments (7). There may also be a healthy survivor bias inherent in longitudinal cohort studies, as the follow-up time in our study was 9 compared with only 3 years in Health ABC. Indeed, a later study in Health ABC (8) using 5-year follow-up data showed an annual decrease in leg strength (-3.2%/year ) more comparable to our findings. To our knowledge, the current study and Health ABC are the only two studies to have published longitudinal measures of body composition and grip strength in men of both African and Caucasian descent. Finally, African-Caribbean men in this study showed an initial decline in lean mass around age 70(3, 9, 10), whereas previous studies have shown an acceleration in muscle or lean mass around age 50. However, these studies were cross-sectional and were comprised mostly of Caucasians.
Examining the association between changes in lean and fat mass with concurrent changes in grip-strength was largely confirmatory – as it was unsurprising we observed that greater declines in whole body and appendicular lean mass and gaining fat mass were significantly associated with greater declines in grip strength (11, 12). However these analyses did yield some interesting results, including that we found it is important to account for body size when examining the association between fat mass and grip strength – as increases in fat mass were associated with better trajectories of grip strength change until weight was included as a covariate. When weight was included as a covariate, we found that decreases in fat mass are associated with better trajectories of grip strength change. We also found that the associations between lean mass and grip strength changes remained constant overtime, but that the association between fat mass and grip strength changes weakened overtime. This suggests that losing fat mass may be more effective at preventing losses of lean mass earlier in the aging process but may not have as great an impact in the oldest old. Indeed, BMI has been shown to be more highly correlated with fat vs. lean mass in older ages (13), and weight loss and having a normal or underweight BMI has been shown to have adverse health affects in older adults (14).
The current study has potential limitations including the reliance on only upper extremity strength measures, and that DXA has been shown to overestimate lean mass, especially in older adults (15, 16). Our study has several notable strengths including the relatively long follow-up period of 9-years, serial measures of body composition and grip strength, wide age range at study entry, assessments of potential lifestyle and medical covariates, and the relatively large sample size. Further, to our knowledge, these are the only longitudinal data describing body composition and strength data across the lifespan in an African ancestry population outside the U.S.
In conclusion, we found that men of African Caribbean ancestry undergo a shift in body composition throughout the adult lifespan – losing lean, while gaining fat mass – resulting in a relatively greater adipogenic phenotypic at older ages. Further, accelerated declines in grip strength with age appeared to precede declines in lean mass by ~10-15 years. We also found that grip strength declines about 2 times fast than lean mass throughout the adult life span. Finally, the declines in lean mass and gains in fat mass were similar to published observations among older African Americans. Additional studies are needed to better define lifestyle, medical and biological factors contributing to body composition remodeling and muscle strength declines across the lifespan in African ancestry populations.
Conflict of interest: The authors have no conflicts of interest to report.
Funding: The research was supported by funding or in-kind services from the Division of Health and Social Services and Tobago House of Assembly, by the National Institute of Arthritis and Musculoskeletal and Skin Diseases (grants AR050107, AR049747) and National Institute of Diabetes and Digestive and Kidney Diseases (grant R01-DK097084). AJS was supported by a career development award from the National Institute on Aging (K01 AG057726).
Acknowlegments: The authors would like to thank the participants of the study and all supporting staff.
1. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. The journals of gerontology Series A, Biological sciences and medical sciences. 2006;61:1059-1064. 61/10/1059 [pii]
2. Santanasto AJ, Miljkovic I, Cvejkus RC, Gordon CL, Bunker CH, Patrick AL, et al. Body Composition Remodeling and Incident Mobility Limitations in African Ancestry Men. The Journals of Gerontology: Series A. 2018:gly067-gly067. 10.1093/gerona/gly067
3. Janssen I, Heymsfield SB, Wang Z, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. Journal of Applied Physiology. 2000;89:81-88. http://jap.physiology.org/content/89/1/81.abstract
4. Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, et al. Leg Muscle Mass and Composition in Relation to Lower Extremity Performance in Men and Women Aged 70 to 79: The Health, Aging and Body Composition Study. Journal of the American Geriatrics Society. 2002;50:897-904. 10.1046/j.1532-5415.2002.50217.x
5. Santanasto AJ, Miljkovic I, Cvejkus RK, Wheeler VW, Zmuda JM. Sarcopenia Characteristics Are Associated with Incident Mobility Limitations in African Caribbean Men: The Tobago Longitudinal Study of Aging. The Journals of Gerontology: Series A. 2019;75:1346-1352. 10.1093/gerona/glz233 %J The Journals of Gerontology: Series A
6. Bunker CH, Patrick AL, Konety BR, Dhir R, Brufsky AM, Vivas CA, et al. High Prevalence of Screening-detected Prostate Cancer among Afro-Caribbeans. The Tobago Prostate Cancer Survey. 2002;11:726-729. http://cebp.aacrjournals.org/content/cebp/11/8/726.full.pdf
7. Winger ME, Caserotti P, Ward RE, Boudreau RM, Hvid LG, Cauley JA, et al. Jump power, leg press power, leg strength and grip strength differentially associated with physical performance: The Developmental Epidemiologic Cohort Study (DECOS). Experimental Gerontology. 2020:111172. https://doi.org/10.1016/j.exger.2020.111172
8. Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. The American Journal of Clinical Nutrition. 2009;90:1579-1585. 10.3945/ajcn.2009.28047
9. Hull HR, Thornton J, Wang J, Pierson RN, Jr., Kaleem Z, Pi-Sunyer X, et al. Fat-free mass index: changes and race/ethnic differences in adulthood. International journal of obesity (2005). 2011;35:121-127. 10.1038/ijo.2010.111
10. Lexell J, Taylor CC, Sjöström M. What is the cause of the ageing atrophy?: Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. Journal of the Neurological Sciences. 1988;84:275-294. http://www.sciencedirect.com/science/article/pii/0022510X88901323
11. Koster A, Ding J, Stenholm S, Caserotti P, Houston DK, Nicklas BJ, et al. Does the Amount of Fat Mass Predict Age-Related Loss of Lean Mass, Muscle Strength, and Muscle Quality in Older Adults? The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2011;66A:888-895. 10.1093/gerona/glr070
12. Cawthon PM, Peters KW, Shardell MD, McLean RR, Dam TT, Kenny AM, et al. Cutpoints for low appendicular lean mass that identify older adults with clinically significant weakness. The journals of gerontology Series A, Biological sciences and medical sciences. 2014;69:567-575. 10.1093/gerona/glu023
13. Gallagher D, Ruts E, Visser M, Heshka S, Baumgartner RN, Wang J, et al. Weight stability masks sarcopenia in elderly men and women. Am J Physiol Endocrinol Metab. 2000;279:E366-375.
14. Santanasto AJ, Goodpaster BH, Kritchevsky SB, Miljkovic I, Satterfield S, Schwartz AV, et al. Body Composition Remodeling and Mortality: The Health Aging and Body Composition Study. The journals of gerontology Series A, Biological sciences and medical sciences. 2017;72:513-519. 10.1093/gerona/glw163
15. Abe T, Patterson KM, Stover CD, Young KC. Influence of adipose tissue mass on DXA-derived lean soft tissue mass in middle-aged and older women. Age (Dordrecht, Netherlands). 2015;37:9741-9741. 10.1007/s11357-014-9741-1
16. Heymsfield SB, Gallagher D, Kotler DP, Wang Z, Allison DB, Heshka S. Body-size dependence of resting energy expenditure can be attributed to nonenergetic homogeneity of fat-free mass. Am J Physiol Endocrinol Metab. 2002;282:E132-138. 10.1152/ajpendo.2002.282.1.E132