
Low grip strength is associated with bone mineral density and vertebral fracture in women
W. G. Dixon,
M. Lunt,
S. R. Pye,
J. Reeve1,
D. Felsenberg2,
A. J. Silman,
T. W. O'Neill on behalf of the European Prospective Osteoporosis Study Group
ARC Epidemiology Unit, Stopford Building, University of Manchester, Manchester, 1 University Department of Medicine, Strangeways Research Laboratory, Cambridge, UK and 2 Department of Radiology and Nuclear Medicine, Free University, Berlin, Germany.
Members of the group are listed in Appendix 1, available as supplementary data at Rheumatology Online.
Correspondence to: T. W. O'Neill, ARC Epidemiology Unit, Stopford Building, University of Manchester, Manchester M13 9PT, UK. E-mail: terry{at}fs1.ser.man.ac.uk
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Abstract
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Objectives. Grip strength has been reported to be associated with bone mass locally at the forearm and also at distant skeletal sites, including the spine and hip. Less is known about the association between low grip strength and risk of vertebral fracture. The aim of this study was to examine the association between low grip strength, bone mineral density at the hip and spine, and vertebral fracture in middle-aged and elderly European men and women.
Methods. Men and women aged 50 yr and over were recruited for participation in a screening survey of vertebral osteoporosis across Europe. Subjects who agreed to take part had an interviewer-administered questionnaire and lateral spinal radiographs performed. Subjects were assessed also for grip strength using a handgrip dynamometer (range 0300 mmHg). A subsample of those recruited had bone mineral density measurements performed at the spine and femoral neck. Subjects had repeat lateral spine radiographs performed a mean of 3.8 yr following the baseline survey. Linear regression analysis was used to determine the association between low grip strength and bone mineral density at the hip and spine. Logistic regression was used to determine the association between grip strength and both prevalent and incident vertebral fracture.
Results. One thousand two hundred and sixty-five men and 1380 women with data concerning grip strength and bone mineral density were included in the analysis. In women, after age adjustment, compared with those with normal grip, those with impaired (231299 mmHg) and low grip (<231 mmHg) had significantly lower bone mass at the spine and femoral neck. In men, those with low grip strength had a lower BMD at the spine and hip than those in the normal group. However, because of the small numbers with submaximal grip strength, the confidence intervals around all estimates included zero. Adjustment for body size and levels of physical activity had little effect on the results. In addition, among women, after adjustment for age, body mass index and physical activity levels, compared with those with normal grip, those with low grip strength had an increased risk of developing incident vertebral fracture (odds ratio = 2.67; 95% confidence interval 1.13, 6.30). Further adjustment for spine bone density had little influence on the association (odds ratio = 2.60).
Conclusions. In women, low grip strength is associated with low bone mineral density at both the spine and hip and an increased risk of incident vertebral fracture. These associations cannot be explained by differences in body size or lifestyle.
KEY WORDS: Grip strength, Bone mineral density, Vertebral fracture, Physical activity, Body size
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Introduction
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Skeletal muscle contraction forces generate large reaction forces during normal activity and such forces are thought to have a trophic or adaptive effect on bone mass locally. An example of this adaptation is an increase in humeral bone mass in tennis players [1, 2]. Most observational studies among non-athletes have reported a positive association between hand grip strength and bone mass locallyat the wrist or forearm [310]. Among women, most studies also suggest a positive relationship with bone mass at other sites including the hip and/or spine [4, 6, 1115]. There are fewer studies in men. Several have reported no statistically significant association between grip strength and bone mineral density (BMD) at the hip or upper limb BMD [1518], though others have reported a positive association with total body bone mineral [19]. In addition, there are few data concerning the relationship with vertebral fracture and the evidence from these studies is conflicting [20, 21]. To our knowledge there are no data concerning the influence of a low grip strength on the occurrence of incident radiographic vertebral fractures. One study has shown an association between grip strength and incident osteoporotic fractures (including vertebral fractures), though the association with vertebral fractures alone was not examined [22].
Our aim was to determine the extent of any association between low handgrip strength and both bone density at the hip and spine, and vertebral fractures in men and women. We looked also at the influence of body size and physical activity variables on these associations.
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Methods
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Subjects
Subjects were recruited for participation in a population screening survey of osteoporosis: the European Prospective Osteoporosis Study (EPOS). In this survey, men and women aged 50 yr and over were recruited from population registers across Europe [23]. Those who agreed to take part had an interviewer-administered lifestyle questionnaire. In the questionnaire, subjects were asked to broadly indicate the most strenuous level of activity carried out daily during each of the following periods of your life for the three age periods 1525, 2550 and over 50 yr (response set: light/moderate/heavy/very heavy) [24]. A glossary was provided giving examples of activities and relating them to an activity level. Current activity levels were assessed by response to the question How much time do you typically spend walking or on a bicycle out of doors each day? (response set: none/some but less than half an hour/half to one hour/more than one hour). Height and weight were measured in all subjects. Each subject gave informed consent to their participation in the manner required by their centre's research ethics committee.
Assessment of grip strength
Grip strength was measured using an Accoson handgrip Limpet dynamometer. The subject's arm was positioned with the elbow flexed and the forearm parallel to the floor. The subject squeezed the inflated cuff between the ball of the hand and the fingers without using the thumb. The maximum value was noted for each squeeze and the highest of three attempts was recorded. The analogue scale ranged from 0300 mmHg. It was possible to go beyond the upper range; if this was the case a value of 300 mmHg was recorded.
Bone mineral density assessment
Hip and spine BMD was assessed in a subsample of participating centres. In these centres, random samples of between 20 and 100% of subjects were invited for bone densitometry. Overall, 52% of subjects at the 10 centres who had data about grip strength and BMD measurements available had both hip and spine BMD measured. Further details about assessment of bone densitometry are described elsewhere [25]. The densitometers in each centre were pencil beam machines made by Lunar, Hologic or Norland and were cross-calibrated using the European Spine Phantom [26, 28]. At least five measurements of the phantom were made on each machine and a two-parameter empirically fitted exponential calibration curve was used to convert measured density values into standardized values, as described by Pearson et al. [27].
Radiological assessment
All subjects had lateral thoracolumbar spine radiographs performed using a standard protocol. Subjects had repeat spinal radiographs performed a mean of 3.8 yr after the baseline survey. The radiographs were forwarded to the radiology coordinating centre in Berlin for evaluation. Both prevalent and incident vertebral fractures were defined according to standard morphometric criteria. For prevalent fractures the McCloskeyKanis criteria were used [29]. Incident fractures were defined if there was evidence of height reduction of 20% or more in any of the three vertebral heights (anterior, middle or posterior) between films and, in the second film, if a vertebra satisfied criteria for a prevalent fracture [30]. The study radiologist also made a clinical (qualitative) assessment about whether an incident vertebral fracture was present.
Statistical analysis
Grip strength was examined as a categorical variable because of the ceiling effect of the dynamometer. Those subjects who obtained a maximal grip strength score of 300 mmHg formed one group, which was labelled normal. Excluding those with maximal grip strength, the remainder were subdivided at the median value of 230 mmHg (which was the same value for men and women), the resulting two groups being labelled impaired (231299 mmHg) and low (<231 mmHg). BMI was calculated by dividing weight by height squared (kg/m2). A lifetime activity score was calculated by summating the scores for the physical activity questions from each of the three age periods. Current physical activity was dichotomised (walking or cycling daily >1 h/<1 h).
Linear regression was used to investigate the association between low grip strength and bone mineral density with adjustments made for age. The analysis was repeated after adjusting for body mass index and both the lifetime activity score and current physical activity levels. Logistic regression was used to look at the association between low grip and the occurrence of both prevalent and incident vertebral fracture. Analyses were undertaken separately in men and women. Statistical analysis was performed using Stata [31].
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Results
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Subjects
In total, there were 1265 men, mean age 64.1 (S.D. = 8.5) and 1380 women, mean age 63.6 (S.D. = 8.2), who had both grip strength and hip/spine BMD measurements available. Of these 2645 subjects, 2553 had baseline lateral spine X-rays and 1389 had baseline and follow-up films.
Baseline characteristics
The baseline characteristics of the subjects are detailed in Table 1. BMD scores were higher for men than women at the femoral neck (0.827 vs 0.726 g/cm2), the trochanter (0.768 vs 0.621 g/cm2), and the spine (1.091 vs 0.935 g/cm2). Men undertook higher levels of physical activity than women. A greater proportion of men were recorded as having normal grip strength (89 vs 37%). In all, 135 (11.0%) of men and 187 (14.1%) of women had evidence of a prevalent vertebral fracture. Amongst those subjects with follow-up radiographs, 11 (1.7%) men and 34 (4.7%) women had evidence of an incident vertebral fracture (either morphometric [40] or qualitative [38]).
Grip strength and BMD
The associations between grip strength category and BMD at the spine and femoral neck are shown in Table 2. Among women, compared with those with normal grip, those with impaired and low grip had significantly lower bone mass at the spine and femoral neck. At the femoral trochanter, bone mass was lower in those with impaired and low grip, though for the former the confidence limits included unity. At all skeletal sites there was also a statistically significant trend towards lower bone mass with lower grip strength (P<0.05). In men, those with both impaired and low grip strength had lower BMD than those in the normal group but, because of the lower numbers of men with submaximal grip strength, the confidence intervals around all the estimates included zero. The absolute difference in bone mass between the three grip strength groups, however, was similar in men and women. Adjustment for body size and levels of physical activity had little effect on the results (Table 2).
Grip strength and vertebral fracture
In both men and women, a low grip strength was associated with an increased risk of prevalent vertebral fracture, though none of these associations was statistically significant (Table 3). Among women, however, after adjusting for age, BMI and physical activity levels, there was an increased risk of incident vertebral fracture among those with a low grip [odds ratio (OR) = 2.67]. Further adjustment for spine BMD did not attenuate risk (OR = 2.60) (Table 3). Among men with a normal grip strength, only nine (1.5%) had evidence of incident vertebral fracture. The corresponding figures for those with impaired and low grip were 1 (2.4%) and 1 (3.5%), respectively. Therefore, the numbers with incident vertebral fracture in the non-normal grip strength groups were too small to permit further analysis.
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Discussion
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In this population-based study we have shown that low grip strength is associated with reduced BMD at both the spine and femoral neck in women. The association could not be explained by differences in body size or levels of physical activity. Among women, low grip strength was also associated with an increased risk of incident vertebral fracture.
There are a number of methodological limitations to be considered in interpreting the results. The response rate for participation in the screening survey in those centres that contributed data to the study was approximately 55% [32]. It is possible that those who declined to participate may have differed with respect to grip strength from those who took part. However, any possible selection factors are unlikely to have influenced the main findings, which are based on an internal comparison of those who participated.
The handgrip dynamometer used in the study had a low ceiling, particularly in men, fully 89% of whom attained the maximum recordable value. Thus, in men, because of the small numbers in the impaired and low grip-strength groups, the confidence intervals were relatively wide. Assessment of grip strength was undertaken without knowledge of the bone density data. Any errors in recording are thus likely to be random and, if anything, would tend to reduce the chance of finding significant biological associations.
In our study the questionnaire instrument concerning current and historical physical activity was also relatively crude. It is possible that the lack of effect of physical activity on the association between bone mass and grip strength was because of the failure of the question to capture accurately the typical recreational, leisure and occupational activities of the subjects. Further studies incorporating more detailed information about the type, frequency and intensity of physical activities undertaken would be required to further explore this.
Our results are consistent with the majority of previous studies among women showing an association between grip strength and bone mass at the spine [4, 6, 11, 13, 14] and the hip [4, 6, 1315]. Zimmerman et al. reported no association between bone mass at the hip and grip strength among a series of postmenopausal women, though the number studied (56) was relatively small [11].
There are relatively few data in men. Our data suggest a reduction in bone mass among those with a low grip strength, the magnitude of the difference from the normal grip group being broadly comparable to that observed in women. Because of the relatively small numbers in both the impaired and low grip groups, however, the study lacked sufficient power to show a statistically significant difference. In other studies, small though non-significant correlations were reported between bone mass at the spine and/or hip; however, the numbers of subjects recruited were small (<40) [4, 15]. In a larger study, Glynn et al. reported a small increase in bone mass at the hip in men with higher grip, though as in our study the confidence intervals embraced unity [16]. In a population-based sample of 348 men, Proctor et al. reported a significant association between grip strength and total body bone mineral [19].
We observed a small though non-significant increase in risk of prevalent vertebral fracture associated with impaired and low grip strength. This is consistent with a recent study in Beijing [21], but differs from the results of a study in Hong Kong, where those in the lowest quartile of grip had a significantly increased risk of prevalent fracture [20]. To our knowledge there are no published data from population surveys concerning the association between low grip strength and incident vertebral fracture. In our study, among women there was an increased risk of incident fracture among those with low grip strength. Whilst it appears that the impaired grip group among women had a reduced risk of incident vertebral fracture, albeit non-significant, the numbers of incident vertebral fractures in this group was small (3, compared with 10 in the normal group and 21 in the low group), making this apparently contradictory finding less robust. The numbers of men with incident vertebral fracture in this data set were too small to permit analysis of an association with grip strength.
Despite the link with low bone mass, the association between low grip strength and incident vertebral fracture in women could not be explained in our study by BMD, suggesting that factors other than bone mass contribute to fracture risk. Such factors may include bone quality, microarchitecture or bone turnover. These could include targeted strengthening of vertebral bodies to resist habitual compressive forces arising from muscular loading that did not translate into a substantial overall BMD increase. Trauma may play a role, though the majority of vertebral fractures are not explained by falls [33]. Low grip may also be a marker for general frailty with decreased reserves in multiple systems, further contributing to increased fracture risk. Thus, grip strength predicts functional limitation, functional decline and mortality in older people [3436]. Further studies are required to confirm these findings and to determine the mechanism by which low grip strength influences fracture risk.
In summary, our data suggest that in women low grip strength is a marker of low BMD at both the spine and hip and that the association is not explained by differences in either body size or level of physical activity. Low grip strength in women is associated with an increased risk of incident vertebral fracture.
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Acknowledgments
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The study was financially supported by a European Union Concerted Action Grant under Biomed-1 (BMH1CT920182) and EU grants C1PDCT925102, ERBC1PDCT 930105 and 940229. The central coordination was also supported by the UK Arthritis Research Campaign, the Medical Research Council (G9321536) and the European Foundation for Osteoporosis and Bone Disease. The EU's PECO programme linked to BIOMED 1 funded in part the participation of the Prague, Piestany and Moscow centres. The central X-ray evaluation was generously sponsored by the Bundesministerium fur Forschung and Technologie, Germany. Individual centres acknowledge the receipt of locally acquired support for their data collection. We would like to thank the following individuals: Aberdeen, UK: Rita Smith; Cambridge and Harrow, UK: Anna Martin, Judith Walton; Oviedo, Spain: J. Bernardino Diaz Lopez, Ana Rodriguez Rebollar.
The authors have declared no conflicts of interest.
Supplementary data
Supplementary data are available at Rheumatology Online.
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Submitted 16 January 2005;
revised version accepted 18 January 2005.