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Aging Clinical and Experimental Research

https://doi.org/10.1007/s40520-018-0933-x

ORIGINAL ARTICLE

Waist circumference is a better predictor of risk for frailty than BMI


in the community-dwelling elderly in Beijing
Qiuju Liao2,4 · Zheng Zheng1,2,6 · Shuangling Xiu2,5 · Piu Chan1,2,3,6

Received: 5 January 2018 / Accepted: 8 March 2018


© Springer International Publishing AG, part of Springer Nature 2018

Abstract
Aim  Obesity is found to be associated with frailty. Body mass index (BMI) and waist circumference (WC) are the commonly
used measures for obesity, the former is more closely related to general obesity and body weight; the latter can more accu-
rately reflect abdominal obesity and is more closely associated with metabolic disorders. In this study, we intend to study
the relationship between frailty, BMI and WC among older people.
Methods  Data were derived from the Beijing Longitudinal Study on Aging II Cohort, which included 6320 people 65 years
or older from three urban districts in Beijing. A Frailty Index derived from 33 items was developed according to Rockwood’s
cumulative deficits method. A Frailty Index ≥ 0.25 was used as the cut-off criteria. BMI was classified as underweight, nor-
mal, overweight, or obese (< 18.5, 18.5–< 24.0, 24.0–27.9, ≥ 28.0 kg/m2, respectively). High WC was defined as WC ≥ 85 cm
in men and ≥ 80 cm in women.
Results  People with a larger BMI (≥ 28.0 kg/m2, 22.6%) or a larger WC (18.5%) were more likely to be frail. People with
normal BMI and overweight people do not suffer from higher prevalence for frailty. In comparison with individuals with
normal BMI (18.5–< 24.0 kg/m2) and normal WC (< 85 cm in men, <80 cm in women), the risk of frailty was higher among
individuals who have normal BMI and large WC (odds ratio 1.68; 95% CI 1.33–2.12), have overweight and large WC (odds
ratio 1.58; 95% CI 1.23–1.96), or have obesity and large WC (odds ratio 2.28; 95% CI 1.79–2.89). In people with normal
WC, only those who are underweight have a higher risk for frailty (odds ratio 1.65, 95% CI 1.08–2.52). In comparison with
BMI, the relation of WC with the risk for frailty was much closer.
Conclusions  Abdominal obesity is more closely associated with incidence of frailty than general obesity in the elderly. Older
adults with large waist circumference are more likely to be frail. Frailty in the elderly might be more closely related to meta-
bolic disorders. WC might be a better measurement to detect frailty than BMI, given its relationship with metabolic disorders.

Keywords  Body mass index · Waist circumference · Frailty · Older adults · Prevalence

4
* Piu Chan Department of Rheumatology, Beijing Institute of Geriatrics,
pbchan@hotmail.com Xuanwu Hospital of Capital Medical University,
Beijing 100053, China
Qiuju Liao
5
qiujumm@sina.com Department of Endocrinology, Beijing Institute of Geriatrics,
Xuanwu Hospital of Capital Medical University,
1
Department of Neurobiology, Beijing Institute of Geriatrics, Beijing 100053, China
Xuanwu Hospital of Capital Medical University, No. 45 6
Key Laboratory on Neurodegenerative Disease of Ministry
Changchun St., Xicheng District, Beijing 100053, China
of Education, and Beijing Key Laboratory for Parkinson’s
2
Department of Geriatrics, Beijing Institute of Geriatrics, Disease, Parkinson’s Disease Center of Beijing Institute
Xuanwu Hospital of Capital Medical University, for Brain Disorders, Beijing 100053, China
Beijing 100053, China
3
Department of Neurology, Beijing Institute of Geriatrics,
Xuanwu Hospital of Capital Medical University,
Beijing 100053, China

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Aging Clinical and Experimental Research

Introduction Dongcheng) in 2009 to exclude the potential bias of envi-


ronmental exposures and life styles between urban and
Population aging has been accelerating in China lead- rural areas. In total, 6320 subjects people were involved.
ing to an increased vulnerability to diseases and physical
frailty [1]. Frailty is a common problem in the elderly and Definition of frailty
increases the risk for disability and raises the demand for
institutional care and even hastens death [2]. In China, The original Frailty Index (FI) consisting of 34 items was
the obesity epidemic is unfolding much faster than it has defined according to the BLSA-II Frailty Index (BLSA-FI)
ever been observed in Western countries, especially so model, on the basis of Rockwood’s accumulation of deficits
in Beijing [3]. With the increase in age, older adults are method [20, 21]. In the current study, BMI was not included
likely to have obesity [4], metabolic syndrome (MetS) in the calculation of the FI, making the FI consisting of only
[5] and diabetes [6]. Reports have shown that obese older 33 items. These deficits were defined as symptoms, signs,
people are at a higher risk of being frail [7]. Metabolic disabilities and diseases deficits [22], including: (1) 12
disorders [8] and diabetes [9, 10] are also found to be chronic conditions, for which the participants were asked
correlated with frailty in the elderly population. Body “Have you ever been diagnosed for the following conditions
mass index (BMI) and waist circumference (WC) reflect by a doctor?” Chronic conditions included hypertension, car-
metabolic problems with different measures, the former diovascular disease, chronic obstructive pulmonary disease
is more closely related to general obesity and weight, and (COPD), diabetes, stroke, dementia, arthritis, tumor, cata-
the latter is more closely associated with abdominal obe- ract, deafness, heart failure and renal failure; (2) 4 functional
sity and metabolic-related diseases (e.g., MetS, diabetes, assessment scales (Mini-Nutrition assessment [MNA] [23],
coronary heart disease et al.) [11–14]. WC is also associ- Tinetti performance-oriented mobility assessment[POMA]
ated with chronic inflammation, oxidative stress and insu- [24], Mini-Mental State Examination [MMSE] [25], Geri-
lin resistance [15, 16], which are also associated with the atric Depression Scale-15 [GDS-15] [26]); (3) 6 disease
risk of frailty [17]. Although previous evidence has shown screening questionnaires (joint pain and inflammation, gout,
that BMI and WC are associated with increased risks for risk of fall, osteoporosis, arterial sclerosis and Parkinson’s
frailty, which of the two is more accurate in predicting disease); (4) 8 self-reported geriatric symptoms (less activ-
frailty is not known. This study intends to investigate the ity, fatigue, weight loss, urinary inconsistence, fecal incon-
relationship of BMI and WC with frailty in community- sistence, memory loss, vision and hearing loss), and (5) 3
dwelling older people in Beijing. blood test measurements (fasting plasma glucose, blood
lipids [triglycerides, total cholesterol, and low and high
density lipoprotein-cholesterols] and uric acid). All items
had less than 5% missing values, and continuous measures
Methods were dichotomized into frailty markers 15 (1 = presence,
0 = absence) based on referenced cutoffs for Chinese. Each
Study participants and design individual’s deficit points were summed and divided by the
total number of deficits considered (in this case 33) to yield
This was a secondary analysis of data from the Beijing an FI with a theoretical range 0–1. The cut-off criterion was
Longitudinal Study on Aging II (BLSA II), which was FI ≥ 0.25 [21], that is to say, a FI of 0.25 or greater indicated
launched in 2009 in Beijing, China, and a follow-up study frailty.
was performed 1 year later, from August 2010 to January
2011 [18]. A multi-stage cluster random sampling method Body mass index and waist circumference
was used to select a representative community cohort aged
55 and older from both urban and rural areas. It found a The BMI was calculated as weight in kilograms divided
12.3% prevalence and a 13% incidence of frailty in com- by the square of the height in meters (kg/m 2). Accord-
munity-dwelling Chinese older adults with the Rockwood ing to the criteria of the Cooperative Meta-analysis
Frailty Index method. Being frail significantly predicted Group of China Obesity Task Force [27], individuals
adverse geriatric outcomes. In a separate analysis, diabe- were classified as underweight, normal, overweight, or
tes was found to be an independent chronic condition that obese (< 18.5, 18.5–<  24.0, 24.0–27.9, ≥ 28.0  kg/m 2,
increased the risk of frailty in community-dwelling older respectively). The WC was measured at the middle point
adults in China [19]. In the current study, we selected par- between the rib margin and iliac crests in a horizontal
ticipants who were 65 or older recruited from only the plane using an inelastic measuring tape. The whole meas-
three urban districts in Beijing (Xuanwu, Xicheng and urement was also completed by well-trained investigators.
Each measurement was repeated twice; if the measured

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Aging Clinical and Experimental Research

values were within 0.5  cm of one another, then their Results


average was calculated. If the difference between the two
measurements exceeded 0.5 cm, then a third measurement Association of BMI and WC with frailty
was conducted. The normal cut-off values for Chinese are
80 cm for females and 85 cm for males [27]. The prevalence of frailty with socio-demographic, lifestyle
and clinical characteristics is shown in Table 1. It shows that
people with obese (BMI ≥ 28.0 kg/m2) were significantly
Statistical analyses more likely to be frail compared with normal BMI individu-
als (22.6 vs 15%, P < 0.0001). In addition, the data show
Chi-square tests were used to analyze the prevalence that people with higher WC (≥ 85 cm in men and ≥ 80 cm
of frailty with different BMI and WC levels. Logistic in women) were significantly more likely to develop frailty
regression model with progressive levels of adjustment compared with those with normal WC (18.5 vs 12.1%,
was used to evaluate the association of BMI and WC P < 0.0001).
with frailty. Because socio-demographic, physical and The odds ratios (OR) with 95% confidence interval (CI)
lifestyle-related factors were associated with frailty, so of the BMI and WC for frailty risks are shown in Table 2.
sex and age were adjusted in Model 1. Model 2 represents People with obese (BMI ≥ 28.0 kg/m2) were associated with
the results adjusted for sex, age, smoking and alcohol an increased risk for frailty (OR 1.37, 95% CI 1.13–1.67,
consumption, number of diseases, living alone, exercise, P = 0.03). After adjusting for sex and age, we observed
sleeping and education. All analyses were performed with that obesity (BMI ≥ 28.0  kg/m2) significantly increased
SAS statistical software version 9.2 (SAS Institute Inc, the risk for frailty (OR 1.41, 95% CI 1.59–1.72, P = 0.008)
Cary, NC, USA). All tests were 2-tailed; P < 0.05 was (model 1). But in the second stepwise multiple regression
considered statistically significant. analysis, further adjusted for parameters (sex, age, smok-
ing, alcohol consumption, number of diseases, living alone,

Table 1  Baseline characteristics of Beijing longitudinal study on aging II


Characteristics Total sample Nonfrail N = 5259 (%) Frail N = 1061 (%) P
N = 6320 (%)

Age (years)
 65–74 3513(55.6) 3067(87.3) 446(12.7) < 0.0001
 75–84 2568(40.6) 2015(78.5) 553(21.5)
 ≥ 85 239(3.8) 177(74.1) 62(25.9)
Gender
 Women 3888(61.5) 3154(81.1) 734(18.9) < 0.0001
 Men 2432(38.5) 2105(86.6) 327(13.4)
Marriage
 Unmarried, widowed or divorced 1497(23.7) 1148(76.7) 349(23.3) < 0.0001
 Married 4823(76.3) 4111(85.2) 712(14.8)
Education
 Less than high school 3644(57.7) 3083(84.6) 561(15.4) 0.0005
 High school/GED/some college 2670(42.3) 2171(81.3) 499(18.7)
BMI (kg/m2)
 Underweight (< 18.5) 199(3.2) 167(83.9) 32(16.1) 0.67
 Normal (18.5–< 24.0) 2379(37.9) 2023(85) 356(15) Ref
 Overweight (24.0–27.9) 2640(42.1) 2212(83.8) 428(16.2) 0.22
 Obese (≥ 28.0) 1051(16.8) 813(77.4) 238(22.6) < 0.0001
WC (cm)
 Normal WC (< 85men, < 80 women) 1658(26.4) 1458(87.9) 200(12.1) Ref
 High WC (≥ 85 men, ≥ 80 women) 4631(73.6) 3772(81.5) 859(18.5) < 0.0001

Chi-square test was used to compare prevalence rates of frailty among subgroups
BMI body mass index, WC waist circumference

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Aging Clinical and Experimental Research

Table 2  Frailty risk according to BMI and WC


Unadjusted Model 1 Model 2

BMI (kg/m2) OR (95% CI) P OR (95% CI) P OR (95% CI) P


Underweight (< 18.5) 1.35 (0.9–2.02) 0.31 1.21 (0.81–1.82) 0.7 1.31 (0.83–2.07) 0.41
Normal (18.5–< 24.0) Ref Ref Ref Ref Ref Ref
Overweight (24.0–27.9) 0.95 (0.8–1.11) 0.005 0.98 (0.83–1.15) 0.04 0.95 (0.79–1.14) 0.03
Obese (≥ 28.0) 1.37 (1.13–1.67) 0.03 1.41 (1.59–1.72) 0.008 1.31 (1.06–1.64) 0.11
WC (cm)
 Normal WC (< 85men, < 80 women) Ref Ref Ref Ref Ref Ref
 High WC (≥ 85 men, ≥ 80 women) 1.65 (1.36–1.98) < 0.0001 1.59 (1.31–1.92) < 0.0001 1.3 (1.05–1.61) 0.01

Model 1: adjusted for sex and age


Model 2: adjusted for sex, age, smoking, alcohol consumption, number of diseases, living alone, exercise, sleeping, and education
BMI body mass index, WC waist circumference

a normal WC but underweight (BMI < 18.5) showed a higher


prevalence of frailty.
Stratification of participants by combination of BMI and
WC categories showed that the risk of frailty was signifi-
cantly higher among individuals who were underweight but
with normal WC (OR 1.65, 95% CI 1.08–2.52, P = 0.04),
normal BMI but a large WC (OR 1.68, 95% CI 1.33–2.12,
P < 0.0001), overweight but a large WC (OR 1.58, 95% CI
1.23–1.96, P < 0.0001), and with both obese and large WC
(OR 2.28, 95% CI 1.79–2.89, P < 0.0001) in comparison
with individuals with normal BMI (18.5–< 24.0 kg/m2)
and normal WC (< 85 cm in men, < 80 cm in women). The
results also showed statistical significance after adjustment
Fig. 1  Association of BMI after taking into consideration WC with with Model 1 or Model 2 (Table 3).
regard to the prevalence of frailty. *P < 0.05

exercise, sleeping, and education), the influence of obesity Discussion


(BMI ≥ 28.0 kg/m2) on frailty showed no statistical signifi-
cance (OR 1.31, 95% CI 1.06–1.64, P = 0.11) (model 2). The current study investigated the relationship between
People with large WC were positively related to increased frailty, BMI and WC in Chinese elderly in the urban com-
risk of frailty (OR 1.65, 95% CI 1.36–1.98, P < 0.0001). The munity. We found that abdominal obesity demonstrated by
results also showed statistical significance after adjustment the measure of WC was more consistently associated with
with Model 1 (OR 1.59, 95% CI 1.31–1.92, P < 0.0001) or an increased risk for frailty even for individuals with a nor-
Model 2 (OR 1.3, 95% CI 1.05–1.61, P = 0.01). mal BMI, suggesting large WC which increased the risk
for metabolic disorders might be more closely related to an
increased risk of frailty in the elderly population. For those
Association of BMI with the prevalence of frailty who had normal BMI or even overweight, the risk for frailty
in relation to WC was not increased if they had a normal WC. These results
suggest that WC is a better predictor of frailty than BMI for
The prevalence of frailty increased with a normal or the elderly.
increased BMI in people with high WC, whereas a lower Many reports demonstrated a close relation between
frequency of frailty was observed in people with a nor- BMI and risk of frailty [7, 28–30]. However, there were
mal or even overweight (BMI 24.0–27.9) when their WC still controversies about the risk of frailty in overweighed
was normal (Fig. 1). On the other hand, as long as a large people. A cross-sectional analysis with 599 community-
WC was present the prevalence of frailty was significantly dwelling women aged 70–79 from the Women’s Health and
increased compared to people with normal BMI and WC, Aging Studies I (1992) and II (1994) cohorts found that
except elderly underweight (BMI < 18.5). Those elderly with being overweight (BMI 25–< 30 kg/m2) did not increase

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Aging Clinical and Experimental Research

Table 3  Frailty risk according to BMI after taking into consideration of WC


WC (cm) BMI (kg/m2)
Underweight (< 18.5) Normal (18.5–< 24.0) Overweight (24.0–27.9) Obese (≥ 28.0)

Unadjusted Normal WC 1.65* Ref 0.91 1.64


(< 85men, < 80women) (1.08–2.52) 126/1096 (0.62–1.34) (0.65–3.91)
n events/total 28/170 37/349 5/35
High WC 1.24 1.68* 1.58* 2.28*
(≥ 85men, ≥ 80women) (0.42–3.59) (1.33–2.12) (1.23–1.96) (1.79–2.89)
n events/total 4/29 230/1283 391/2291 232/1016
Model 1 Normal WC 1.52* Ref 0.96 1.49
(< 85men, < 80women) (1.2–2.16) (0.65–1.42) (0.6–3.69)
High WC 1.04 1.66* 1.56* 2.25*
(≥ 85men, ≥ 80women) (0.49–2.97) (1.31–2.1) (1.25–1.94) (1.75–2.87)
Model 2 Normal WC 1.72* Ref 1.1 1.37
(< 85men, < 80women) (1.07–2.89) (0.72–1.69) (0.51–3.68)
High WC 0.8 1.45* 1.27* 1.77*
(≥ 85men, ≥ 80women) (0.27–2.81) (1.12–1.88) (1.13–1.62) (1.34–2.32)

Model 1: adjusted for sex and age


Model 2: adjusted for sex, age, smoking, alcohol consumption, number of diseases, living alone, exercise, sleeping, and education
BMI body mass index, WC waist circumference
*P < 0.05

the risk of frailty [29]. However, results from 40,657 their findings, and, in fact, there were quite other studies
women aged 65–79 who participated in the Women’s that also replicated the results [34, 35].
Health Initiative [30], and were followed up for 3 years, As people grow old, muscle mass and strength decrease,
confirmed that being overweight could markedly increase and body fat increases, and BMI is the most commonly used
the risk of frailty. Although it is now known the exact anthropometric measurement to assess adiposity [36, 37].
cause of this discrepancy, our study showed that being However, our study has shown that overweight individuals
overweight (BMI 24.0–27.9 kg/m2) increased the risk of did not have an increased risk for frailty if they had a normal
frailty only for those with increased but not normal WC, WC, only those with a larger WC had an increased risk for
suggesting that it is the abdominal obesity that is associ- frailty even if with a normal BMI. These results suggest that
ated with frailty. Since we have adjusted sex and age in the WC is a better indicator of frailty than BMI. We speculate
analysis, it is less likely that this relationship between WC that WC is associated with abdominal obesity or more vis-
and frailty was only relevant for oldest old. ceral fat, and with metabolic disorders [17, 35]. Fat cells can
Despite numerous studies focused on relationship secrete cytokines such as leptin, adiponectin, resistin, TNF,
between BMI and frailty, there were only few on WC and IL-6 and visfatin, which play important roles in metabolism,
frailty. There were quite few studies on relationship of inflammation, blood coagulation, fibrinolysis, endothelium
frailty related to metabolic disorders. Metabolic disorders function and transmitting metabolic information between
are well known to be closely related to cardiovascular dis- different organs [17, 31, 35, 38, 39]. Abdominal obesity
eases and diabetes. Older people with metabolic disorders exerts an anti-insulin effect, which leads to abnormal glu-
are more likely to suffer from chronic diseases and are cose tolerance. Moreover, people with abdominal obesity
prone to suffer adverse health outcomes [31, 32]. One of also suffer from chronic stress and chronic inflammation
the most accepted indicators of abdominal obesity is WC. [40]. All these factors have been proposed to mediate the
To some extent, it reflects how fats are distributed across mechanisms leading to frailty [35]. Furthermore, increased
the body. Although CT or MRI are more precisely discern WC has also suggested to be markers of oxidative stress,
specific components of body composition (e.g., visceral independent from BMI [16]. Excessive and unopposed oxi-
versus subcutaneous adipose tissue or ectopic fat in tis- dative stress may be the core mechanism leading to age-
sues and organs) [33], WC is widely used for its ease of associated frailty [41]. Increased overall adiposity is a factor
measurement. The earliest report on frailty and abdomi- linked to higher rates of depression, cognitive decline [42]
nal obesity was a British cross-sectional study, suggested and osteoporosis [43] in the elderly, ailments which all are
that a large WC was closely related to frailty, even among components related to frailty. BMI is affected by many fac-
underweight people [28]. Our results are consistent with tors, such as body size (humpback in the elderly), skeletal

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Aging Clinical and Experimental Research

and muscular weight, and it does not reflect the body fat Ministry of Science and Technology of China (2012AA02A514,
distribution [16]. In the elderly in particular, body weight 0S2012GR0150, 2012ZX09303-005).
could be an important indication of their health status, more
weight (a higher BMI) may demonstrate a better preserve Compliance with ethical standards 
or healthy as compared to the adults. While larger WC may
Conflict of interest  No potential conflicts of interest were disclosed.
suggest increased risk for metabolic disturbance even when
the elderly with a normal body weight. Therefore, these data Ethics approval  All procedures performed in studies involving human
support that people with large WC are more prone to be frail. participants were in accordance with the ethical standards of the
It is interesting to note that we found those who were Research Ethics Committee of Xuanwu Hospital, Capital Medical
University. In addition, this study was performed in accordance with
underweight but with a normal WC had a higher risk for the ethical principles of the Declaration of Helsinki.
frailty, while the risk for frailty decreased when WC was
increased. Our results are different from previous report Informed consent  Written informed consent was obtained from all
by Hubbard et  al. that found people with large WC but participants.
underweighted had an increased risk for frailty [28]. These
contradicted results might be explained by possible differ-
ent mechanisms leading to frailty between underweighted
and overweighed. The low BMI may represent low reserve References
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