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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES

For a given level of adiposity, greater lower body circumferences appear to exert a protective effect on several disease outcomes including cardiovascular disease and diabetes; however, the independent associations between extremity circumferences and mortality have not been widely investigated. The purpose of this study was to determine the independent and shared influences of upper- and lower-body circumferences on the risk of mortality in a population-based sample of adults. The sample included 10,638 adults 20–69 years of age (5,012 men; 5,626 women) from the nationally representative 1981 Canada Fitness Survey (CFS), who were monitored for over 12 years for mortality. BMI was calculated from measured height and weight. Waist, hip, thigh, calf, and upper arm circumferences were measured using a flexible, nonelastic anthropometric tape. Sex-specific proportional hazards regression models were used to evaluate the relationship between standardized values (Z-scores) of extremity circumference measures, waist circumference (WC) and mortality. Age, smoking status, alcohol consumption, and leisure-time physical activity were collected by questionnaire and were included as covariates. During 131,563 person-years of follow-up, there were 340 deaths in men and 231 in women. After mutual adjustment, WC was positively associated with mortality whereas arm, thigh, and calf circumferences were significantly protective in men, and arm and thigh circumferences were protective in women. In conclusion, waist and extremity circumferences appear to have opposite, independent effects on mortality in this sample of Canadians. Independent of BMI and WC, men and women with larger extremity circumferences had a lower risk of mortality.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES

Obesity is a major risk factor for a multitude of chronic conditions as well as for premature mortality (1). Thus, as the prevalence of obesity increases around the world, so does its relative importance as a modifiable risk factor for improving public health. An international classification system based on the BMI is now widely used to identify individuals with elevated obesity-related health risks. Yet, the BMI is not without limitations. For example, the BMI cannot differentiate between lean and fat mass, nor can it account for differences in relative fat distribution. These are important limitations given that the localization of fat mass in the abdomen is an independent predictor of premature death (2), and that fat and lean mass have previously been shown to have differential effects on the risk of mortality (3,4,5).

Achieving a more accurate characterization of health risk using anthropometry will advance the descriptive and analytic epidemiology of obesity and consequently improve clinical risk stratification among the growing number of individuals classified as overweight or obese on the basis of BMI. Although elevated waist circumference (WC) confers additional health risk at any level of BMI (6), smaller hip and thigh circumferences have been identified as significant predictors of cardiovascular disease risk factors (7,8,9) and type 2 diabetes mellitus (8,10,11). Moreover, hip circumference has been shown to independently influence longevity among participants of the Gothenburg Women's Health Study (12) and in older adults (50–70 years) enrolled in the prospective study of ‘Diet, Cancer, and Health’ (13). Yet, to date, few studies have examined the independent influence of additional upper- and lower-body circumferences on mortality rates, particularly in the general population.

Recently published findings by Wannamethee et al. (14) reported a decreasing risk of all-cause mortality across increasing quintiles of mid-arm muscle circumference in older men (60–79 years of age), independent of adiposity. Similarly, findings based on representative samples of men and women from the NHANES I and II epidemiologic follow-up studies also showed differential effects of arm circumference and BMI on mortality rates (4,15). The purpose of this investigation was to examine the influence of upper- and lower-body circumferences on the risk of mortality, independent of BMI and waist circumference in a large, population-based sample of Canadian adults.

Methods and Procedures

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES

Sample

The 1981 Canada Fitness Survey (CFS) was based on a representative sample of the Canadian population, including individuals from urban and rural areas of every Canadian province (16). Approximately 3% of the total population was excluded, including Aboriginal people living on reserves, students living in school dormitories, armed forces personnel living on bases, and residents of the Territories and remote areas. A total of 23,400 people between the ages of 7 and 97 years participated in the survey in one way or another. The overall sample considered here includes 10,638 adults (5,012 men; 5,626 women) 20–69 years of age; however sample sizes vary from measure to measure due to missing values for some participants. Participants were given an explanation of the testing protocol and informed consent was obtained before participation.

Exposure variables

Anthropometric dimensions were taken according to the standardized procedures of the CFS during household visits in 1981 (17), and a quality assurance program was conducted to ensure ongoing precision and accuracy of measurement. Briefly, stature was measured using a Harpenden tape to the nearest 0.1 cm and body mass was measured to the nearest 0.1 kg using a standing beam balance scale (Seca, Columbia, MD). BMI was calculated as weight (kg)/height (m)2. Circumference measurements were taken on participants in the standing position and were made to the nearest 0.1 cm using a flexible, nonelastic anthropometric tape. WC was measured at the point of noticeable waist narrowing. In cases of indeterminant waist narrowing, WC was measured at the estimated lower level of the twelfth or lower floating rib. Hip circumference was measured at the level of the symphysis pubis and the greatest gluteal protuberance. The waist-to-hip ratio (WHR) was calculated as WC divided by hip circumference. Thigh circumference was measured on the right thigh, one centimeter below the gluteal line. Calf circumference was measured on the lower right leg at the point of maximal circumference. Finally, the upper arm circumference was measured on the right arm while flexed in a comfortable raised position. The measurement was taken at the widest girth while the muscle was contracted. Arm, thigh, and calf circumference measures were also used to derive ratio measures (waist-to-arm, WTA; waist-to-thigh, WTH; waist-to-calf, WTC) in a manner similar to the WHR.

Covariates

Age, smoking status, alcohol consumption, and leisure-time physical activity were collected by questionnaire at baseline and considered as covariates. Age was determined from birth and observation dates and coded as a continuous variable. The smoking status of participants was coded as nonsmokers, former smokers, or current smokers. Alcohol consumption was categorized according to average intake and frequency of consumption (abstainer; <10 drinks/month; 10–50 drinks/month; >50 drink/month) and included in the regression models as a series of dummy variables.

Leisure-time physical activity levels were assessed using a questionnaire modeled after the Minnesota Leisure Time Physical Activity Questionnaire (18) that collected information about physical activities performed over the preceding 12 months. A list of physical activities was provided and respondents indicated the number of occasions and the average duration of the activity bouts. Average daily leisure-time activity energy expenditure (AEE) was calculated as follows:

  • image

where Ni is the number of times the activity was performed, Di is the average duration in hours of the activity, and METSi was the estimated energy cost of the activity (kcal·kg−1·h−1). Due to significant skewness of the original AEE variable, the natural logarithm of (AEE +1) was used in all regression analyses (with one added to obtain only nonnegative values). For ease of interpretation, descriptive data are presented in original units.

Ascertainment of mortality

The CFS database was linked to the Canadian Mortality Database at Statistics Canada. The Canadian Mortality Database contains all recorded deaths in Canada since 1950, and is regularly updated using death registrations supplied by every province and territory. Record linkage was performed using computerized probabilistic techniques, and the potential for death linkages to be missed using the method employed by Statistics Canada is quite small (19,20). All deaths occurring from the end of CFS data collection (1981) through 31 December 1993 were included in the present analysis. A total of 571 deaths occurred during 131,563 person-years of follow-up (mean: 12.4 years).

Statistical analysis

All data management and analyses were conducted using SAS software version 9.1 (SAS, Cary, NC). Differences in baseline characteristics between men and women were tested by Student's t-tests for continuous variables and by χ2-tests for proportions. Partial correlations between all of the anthropometric variables were computed, adjusting for age. Sex-specific proportional hazards regression models were used to evaluate the relationship between standardized values (Z-scores) of BMI, WC, hip, and extremity circumferences (thigh, calf, and arm) with all-cause mortality rates. Initially, all models included age as a covariate and subsequent models included the effects of smoking status, alcohol consumption, and leisure-time physical activity. The BMI was then added to selected models. Second order polynomial terms were systematically tested to evaluate nonlinear relationships between anthropometric measures and mortality. Only the squared term for hip circumference reached statistical significance among women (P = 0.027); therefore, these terms were not retained in the final models. Potential effect modification by sex was also evaluated by adding appropriate product terms to general regression models that included the entire sample. To investigate the effect of eliminating disease assumed to be present at baseline, the primary analyses were subsequently repeated after exclusion of individuals who died within the first 2 years of follow-up (n = 61).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES

Table 1 provides the baseline characteristics of the sample. Women were significantly older than men (mean age: 38.5 years vs. 38.0 years) at baseline. Men and women also differed significantly with respect to all anthropometric variables. Women had lower BMI, WC, hip circumference, calf circumference, and arm circumference values, but higher thigh circumferences compared with men. Ratio measures (WHR, WTH, WTA, and WTC) were also lower among women than men. Women were less likely to be current smokers or heavy drinkers at baseline and reported significantly lower levels of leisure-time physical activity compared with men. All of the anthropometric variables exhibited significant positive correlations with each other in both men and women and the partial correlation coefficients (adjusted for age) are shown in Table 2. The derived ratio scores generally had the weakest correlations with other variables, with the exception of the relationship between WHR and WC (data not shown).

Table 1.  Baseline characteristics of men and women 20–69 years of age from the 1981 Canada Fitness Survey
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Table 2.  Partial correlation coefficients between baseline anthropometric measures among men (shaded) and women (nonshaded) in the CFS, adjusted for age
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After 13 years of follow-up, there were 340 deaths (132 cardiovascular disease, 114 cancer, 94 other causes) in men and 231 deaths (49 cardiovascular disease, 114 cancer, 68 other causes) in women. Table 3 summarizes the age-adjusted hazard ratios derived from Cox regression analysis for each of the anthropometric measures in relation to total mortality. After adjusting for all covariates, BMI, WC, and the WHR were significant positive predictors of all-cause mortality in women but not men. In contrast, thigh, calf and arm circumference were inversely associated with mortality in men but not women. Hip circumference was not a significant predictor of mortality in either sex. WTH, WTC, and WTA ratios were each a strong positive predictor of mortality in men and women. Sex was a significant (P < 0.05) effect modifier of the associations between both arm and calf circumference and all-cause mortality, but not for any other variables. For the sake of comparison, risk ratios were also calculated for cardiovascular and cancer-related deaths. In both cases, the direction of the associations were the same as for all-cause mortality; and the magnitude of the protective effect associated with hip, thigh, calf, and arm circumferences was surprisingly robust. However, some of these associations failed to reach statistical significance.

Table 3.  Hazard ratios for all-cause mortality associated with anthropometric markers over 13 years follow-up of participants in the 1981 Canada Fitness Survey
inline image

After adjustment for WC, arm, hip, thigh and calf circumferences were inversely associated with all-cause mortality in men and in women, independent of BMI and the other covariates (Figure 1). For a given WC, each standard deviation in arm circumference was associated with a significantly lower risk of mortality of the same magnitude in both men (HR: 0.75, 95% confidence interval (CI): 0.62–0.90) and women (HR: 0.75, 95% CI: 0.59–0.95). Likewise, the risk reduction associated with each standard deviation of thigh circumference was also of a similar magnitude in both sexes (men: 0.79, 95% CI: 0.67–0.93; women: 0.81, 95% CI: 0.67–0.98). By comparison, the hazard ratio associated with each standard deviation of hip and calf circumferences were 0.98 (95% CI: 0.79–1.20) and 0.78 (95% CI: 0.66–0.92) in men and 0.81 (95% CI: 0.63–1.04) and 0.86 (95% CI: 0.73–1.02) in women, respectively (Figure 1). No significant association was apparent between BMI and mortality in models that included WC in addition to any of the upper or lower-body circumferences.

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Figure 1. Hazard ratios for all-cause mortality per 1 s.d. of (a) hip, (b) thigh, (c) calf and (d) arm circumference in men and women. The results for each panel are from a separate model. In addition to WC, all models included age, BMI, smoking status, alcohol consumption, and leisure-time physical activity as covariates. The error bars denote 95% confidence intervals.

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The exclusion of deaths occurring within the first 2 years of follow-up (n = 61) had no meaningful effects on the results reported above. With the exception of thigh circumference in women (P = 0.0656), arm, calf, and thigh (in men) circumferences remained significantly predictive of all-cause mortality in models that included WC, BMI, and all other covariates.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES

The purpose of this study was to examine the independent effects of WC and multiple upper- and lower-body circumferences on mortality rates in a large, representative sample of adults. Despite the positive associations between all of the circumferences and mortality when considered separately, the mutually adjusted associations of waist and these additional circumferences occurred in opposing directions. Therefore, the results confirm the elevated risk of premature mortality associated with abdominal adiposity reported elsewhere (5,21) but also indicate a substantial protective effect of larger extremity circumferences, particularly thigh, calf, and arm, independent of BMI.

The observed protective health effects associated with larger upper and lower-body circumferences in this study are consistent with a limited number of previous reports. In particular, it has been shown that a larger hip circumference for a given WC is inversely associated with cardiovascular and metabolic morbidities (7,9,10,11,22), as well as with mortality (12,13). Similarly, an inverse association between upper arm circumference and mortality, independent of BMI, has previously been shown in female (15) and male (4) participants of NHANES I and II. In older men (61–79 years) from the British Regional Heart Study (14), mid-arm muscle circumference demonstrated a strong inverse association with mortality that persisted after adjustment for multiple indicators of ill health including FEV1, albumin, self-reported poor health, preexisting cancer, diabetes or cardiovascular disease. Moreover, the adverse consequences of low arm circumference in that sample were observed irrespective of BMI and WC, and in active as well as inactive men. To our knowledge, the current investigation is the first to demonstrate a protective effect of multiple upper- and lower-body circumferences on mortality in a single population-based sample.

It is postulated that these inverse associations between upper- and lower-body circumferences and health risk may be owed to a greater accumulation of subcutaneous adipose tissue, greater lean-body mass, or a combination of these factors in the periphery (23,24,25,26). Attempts to estimate the muscle cross-sectional area in the arm and lower leg by correcting for skinfold thickness (27) among participants of the CFS did not yield hazard ratios that were meaningfully different from those of the simple circumferences. However, major body mass compartments have been shown to have differential effects on mortality in select populations (3,4,5). For example, higher abdominal fat (sagittal diameter adjusted for trunk skinfold thicknesses) was a significant predictor of all-cause, cardiac and cancer deaths in the Paris Prospective Study of middle-aged men, whereas greater muscle mass (sum of mid-arm and mid-thigh circumferences adjusted for extremity skinfold thicknesses) was inversely associated with all-cause and cancer deaths, and low extremity subcutaneous fat was associated with greater cancer mortality (5).

Because the CFS did not employ imaging technology, it is difficult to accurately discern the degree to which the effects of larger extremity circumferences observed in this study reflect variation in bone structure, muscle mass, and/or subcutaneous fat mass. Using whole-body magnetic resonance imaging, Kuk et al. (26) recently reported that for a given WC, men and women with larger hip and thigh circumferences have higher quantities of total, lower body, and abdominal subcutaneous adipose tissue, greater skeletal muscle mass, and less visceral adipose tissue. The authors suggested that smaller lower-body circumferences may therefore represent a phenotypic companion to visceral adipose tissue accumulation, further contributing to a body shape phenotype at high risk of cardiometabolic complications.

Owing to sample size limitations, an in-depth analysis of disease-specific causes of death was not possible in this investigation. However, the direction of the associations and the magnitude of effect associated with larger extremity circumferences for a given BMI and WC appeared consistent for cardiovascular and cancer-related deaths in supplemental calculations. Thus, although dominant antiatherogenic properties of peripheral subcutaneous adipose tissue, particularly of the lower-body, have been previously highlighted in elderly women (24), the protective effects of larger extremity circumferences may not be mediated solely through cardiometabolic pathways. Indeed, results from the Paris Prospective Study demonstrated elevated risk of cancer mortality associated with low muscle mass and with low subcutaneous fat in the arm and thigh region of native-born Frenchmen (5). More focused efforts to elucidate the mechanistic link(s) through which extremity circumferences exert their influence on mortality are therefore warranted and will be an important area for future study. Further investigations in this area may also help to clarify potential differences in the relative importance of body composition in the upper compared with lower limbs with respect to specific health outcomes.

There are several strengths and weaknesses of the current investigation that warrant discussion. The large, representative sample of Canadian men and women and the prospective design are marked strengths, as is the direct measurement of all anthropometric indicators. Unfortunately, no data are available with respect to changes in anthropometric markers over the follow-up period, which would have allowed the analyses to be refined further. Since excluding participants who died within the first 2 years of follow-up did not appreciably change the results; it appears that the observed relationships were not confounded by changes in body composition secondary to undiagnosed disease present at baseline.

The measurement protocols employed in the CFS used measurements of proximal thigh circumference which may have been uncomfortable for some individuals, resulting in missing data for ∼2% of participants. Alternative protocols for thigh circumference take measurements at the mid-thigh (mid-way between the inguinal crease and the proximal border of the patella) (28) which may be more culturally acceptable in many cases. Based on our results, we suspect that the observed association between thigh circumference and mortality would be comparable between these anatomical locations of thigh measurement.

The relevance of both the composition (i.e., fat and lean components) and localization of body mass in explaining health outcomes are increasingly recognized. This study adds important new information regarding the influences of extremity circumferences on the risk of mortality, above and beyond that captured by overall and central adiposity as measured by BMI and WC. It also adds to the growing discussion with regards to the characterization of high-risk phenotypes and the value of anthropometric measurements for clinical risk stratification. The strong inverse associations between extremity circumferences and mortality observed in this study suggest that extremity circumferences taken in conjunction with WC may serve some utility in research and clinical settings.

A better understanding of the associations observed in this study and the physiological mechanism(s) underlying them will require concurrent assessment using anthropometry in conjunction with sophisticated imaging techniques that will allow specific types of tissues to be accurately differentiated. Moreover, there is some evidence that muscle morphology, rather than muscle mass alone, may be of greater consequence for health outcomes (29,30). Potential differences in this regard also merit further investigation. Despite practical challenges, studies to carefully assess regional body composition may yield novel and useful insights into the relationship between body composition and mortality.

Acknowledgment

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES

Funding for the record linkage at Statistics Canada was provided by Health Canada. C.M. is supported by a Canada Graduate Scholarship from the Canadian Institutes of Health Research. P.T.K. is supported, in part, by the Louisiana Public Facilities Authority Endowed Chair in Nutrition.

REFERENCES

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods and Procedures
  5. Results
  6. Discussion
  7. Acknowledgment
  8. Disclosure
  9. REFERENCES
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