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1 MRC National Survey of Health and Development, Department of Epidemiology and Public Health, Royal Free and University College London Medical School, United Kingdom.
2 MRC Environmental Epidemiology Unit, University of Southampton, United Kingdom.
Address correspondence to Diana Kuh, PhD, MRC National Survey of Health and Development, Department of Epidemiology and Public Health, Royal Free and University College London Medical School, Gower Street Campus, 1-19 Torrington Place, London, U.K. E-mail: d.kuh{at}nshd.mrc.ac.uk
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Methods. Handgrip strength and body size were measured in a representative British sample of 1406 men and 1444 women 53 years old with prospective childhood data. Normal regression models were used to examine the effects of birth weight, postnatal height and weight gain before 7 years and between 7 and 15 years, motor milestones and cognitive ability on grip strength at age 53, taking account of lifetime social class, current physical activity, and health status.
Results. Birth weight and prepubertal height gain were associated with midlife grip strength, independently of later weight and height gain and other determinants. Pubertal growth was also independently associated with midlife grip strength; for men weight gain during puberty was beneficial, whereas for women it was height gain. Those participants with earlier infant motor development had better midlife grip strength, which was partly confounded by the growth trajectory.
Conclusions. This study showed that components of prenatal, prepubertal, and pubertal growth have long-term effects on midlife grip strength. To the extent that these associations are modifiable, interventions in childhood that help to build muscle mass and strength, such as increased physical exercise, may have long-term beneficial effects on adult muscle strength and may help to prevent sarcopenia, disability, and frailty in later life.
Using prospective data on the same cohort, we now examine the effects of height and weight trajectories from birth to adult life on midlife muscle strength to assess the relative importance of prepubertal growth, pubertal growth, or subsequent weight or height gain. These trajectories may be better markers of muscle growth than are single measurements of size. If early postnatal development of muscle fibers has critical effects on later strength, we hypothesised that prepubertal growth would be positively related to midlife muscle strength, independently of later changes in body size or other determinants of grip strength. We hypothesized that, if muscle growth during puberty has a critical effect, pubertal growth and timing of puberty would be independently related to midlife strength. This effect could vary by gender, as there is evidence of a greater influence of sex hormones on muscle strength in males than in females during puberty (11). As muscle strength is dependent upon neural control as well as muscle size, we also investigated whether age at reaching motor milestones and childhood cognitive ability, which are both regulated by the central nervous system, were associated with midlife strength. We controlled for childhood growth to test whether any associations were explained by muscle size. We controlled for later changes in adult body size, lifetime socioeconomic conditions, and current health status to test whether childhood growth and development are critical for adult muscle strength, or whether they represent the beginning of a pathway through life that promotes strength because of various protective life experiences.
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METHODS |
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At the most recent home visit at age 53 years, voluntary muscle strength was measured isometrically using an electronic handgrip dynamometer (13). The dynamometers were calibrated at the start using a back-loading rig; they are accurate, linear, and stable to ±0.5 kg. There were two sizes of handle for the transducer to accommodate different hand sizes. Each nurse interviewer was taught to give strong verbal encouragement to elicit maximal performance from the participants. Two values were recorded for each hand; the highest was used in the analyses. The intra-individual test–retest variability for maximal voluntary tests of strength in those participants unused to such measurements is approximately ±9% (14). We obtained valid measures of grip strength for 1406 men and 1444 women. The remaining 79 study members were either not examined, were unable to take the test because of chronic disease or disability, or had invalid scores.
Heights and Weights
Birth weight (kg), height (cm) and weight (kg) in childhood (at ages 2, 4, 7, and 15), height (cm) at age 53, and weight (kg) at 26, 36, 43, and 53 years were measured using standardized protocols (15), except at age 26 years when they were self-reported. Yearly rates of weight change were derived between 0 and 7, 7 and 15, and 15 and 53 years ("weight velocities"), and yearly rates of height change were derived between 2 and 7, 7 and 15, and 15 and 53 years ("height velocities"), because birth length was not available. The exact differences in age in months at measurement were used in the denominator. All heights, weights, and weight and height change variables were transformed into standardized scores with a mean of 0 and a standard deviation of 1.
Motor Developmental Milestones
Ages (in months) at first standing and at walking unaided were recalled by the survey member's mother at age 2 years. The modal age for standing and walking was 12 months.
Childhood Cognitive Ability
Tests of reading comprehension (sentence completion), pronunciation, vocabulary, and nonverbal reasoning (picture intelligence) designed especially for the study by the National Foundation for Educational Research in England and Wales were taken at ages 8, 11, and 15 years (16). The average score of the tests taken at the earliest age was used in this analysis as a marker of early childhood cognitive ability and, as with the growth measures, was transformed into a standardized score.
Timing of Puberty
During medical examinations carried out by school doctors for each participant at age 11 and 15 years, the survey member's mother was asked whether their daughter had begun menstruating. For those participants who began menstruating after the last examination or for whom these data were missing (n = 104), age at menarche was recalled on a postal questionnaire completed at age 48 years. For the analysis, age at menarche was classified as occurring at 11 years or earlier, 12 years, 13 years, or 14 years or later. The stage of pubertal development of boys was determined by school doctors at each male participant's medical examination at age 15, and classified as "mature" (advanced development of genitalia, profuse pubic and axillary hair, and voice broken), "advanced" (advanced development of genitalia but not fully mature on according to at least one other marker), "early" (early development of genitalia and some pubic or axillary hair or voice starting to break), or "infantile" (infantile or early adolescent genitalia but no pubic or axillary hair and voice not broken).
Potential Confounders
Potential confounders were two measures of physical activity and four measures of health status at age 53 that were found to be associated with grip strength in men or women in this cohort, and were described in detail previously (13). General physical activity distinguished between those participants who reported taking part in sports or other physical activities in their leisure time in the previous 4 weeks and those who did not. Specific use of strong hand movements in vigorous activities was assessed on a five-point scale of frequency from never to several times a day. Those participants with disabling or life-threatening conditions (diabetes, cancer, epilepsy, or cardiovascular disease) or with severe respiratory or musculoskeletal symptoms were identified from standardized questions, and clinical signs of hand osteoarthritis were identified by trained nurses using standardized criteria (13). We also controlled for socioeconomic conditions using the British Registrar General's classification of social class, grouped to distinguish between the manual or nonmanual social classes, and based on father's occupation in childhood and participant's occupation in adult life.
Analysis
First, grip strength was examined in men and women separately in relation to the standardized heights and weights at all available ages and timing of puberty using separate multiple regression models for each age and adjusting only for height at 53 years. In these models, the maximum available sample was used. Sex interaction terms were added to models including both men and women to test whether the effects of growth on grip strength differed by gender. We ran a multivariable model using 1604 men and women with complete data, including birth weight, height at age 2 and the weight and height velocities, and sex and sex interaction terms (where appropriate), and controlled for adult determinants of grip strength. Second, we examined height- and sex-adjusted grip strength in relation to age at reaching motor milestones and early cognitive ability, and tested whether any relationships observed were explained by birth weight, the weight velocities, or adult factors in a subsample with complete relevant data. All relationships with continuous explanatory variables were tested for deviation from linearity by adding a quadratic term to the regression models.
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RESULTS |
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The relationships between the weight and height velocities and grip strength in the subsample with complete growth data are shown in Table 2, model 1. Birth weight, height at age 2, and height gain between 2 and 7 years and 15 and 53 years were positively related to grip strength. In addition, height gain between 7 and 15 years was associated with grip strength in women, whereas weight gain between 7 and 15 years was associated with grip strength in men. These estimates hardly changed after controlling for health status, physical activity, and social class (Table 2, model 2). There was no additional effect of timing of puberty in these models (data not shown).
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DISCUSSION |
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The effect of prepubertal growth on grip strength probably reflects muscle growth and tracking of muscle size. There is growing recognition that the number of muscle fibers is not fixed by the time of birth as previously believed, and evidence is emerging for the role of satellite cells in postnatal growth and regeneration (17). Prepubertal muscle growth may therefore include an increase in muscle fiber number as well as size.
There are at least two possible explanations for the gender difference in the effects of pubertal height and weight gain on grip strength that are probably related. One is that the muscle development is greater in boys than in girls at puberty because of the different influence of sex hormones (8) or synergism between growth hormone and androgens (18). This may be a reason for the higher proportion of lean to fat tissue in males than in females, so body weight is a better marker of muscle mass in males. Girls carry proportionately more body fat than do boys (19–21), and the percentage of body fat increases with age in girls but remains relatively steady in boys (19,20). Pubertal height gain rather than weight gain may be a better marker of muscle development in women and may explain why this component of the height trajectory remained associated with grip strength even after adjusting for the rest of the trajectory.
The positive effect of motor milestones on grip strength was in part due to the faster height and weight gain of persons with advanced development. Any remaining effect could reflect initial differences in structural and functional maturation of brain motor systems that are somehow sustained (22). A recent study in a Finnish birth cohort to age 35 has shown, for the first time, a long-term normative continuity between timing of motor development and anatomical integrity of adult motor systems (22). To our knowledge, motor milestones have not been previously linked to adult grip strength. The inverse U-shaped effect of early cognitive ability on later grip strength was unexpected and remains unexplained.
Our study had a number of limitations. The growth trajectories were inevitably limited by the ages when height and weights were measured and, as rates of maturation vary considerably between individuals, parameters of growth such as peak growth velocity cannot be derived. We were, however, able to characterize prenatal, prepubertal, and pubertal growth, showing effects of each of these parameters on later grip strength. The analyses using the growth trajectory were also restricted to participants with complete data, and reduced the statistical power of the study. There were, however, few differences between participants with and without complete data and no reason to expect that relationships between childhood growth and midlife grip strength should vary between the two samples. Measures of body composition during growth and more refined measures of the development of motor competence would be advantageous; studies of younger cohorts (23), which are better characterized in these ways, eventually will be able to evaluate these effects on adult strength. The relative proportions of fat and lean mass, however, may have changed in these cohorts compared to our cohort where there was little childhood obesity. The effects of childhood growth and development on adult performance were not strongly attenuated by adjustment for socioeconomic conditions, physical activity, and health status. Residual confounding, however, remains a possible explanation for the observed associations either because these covariates were measured imprecisely or because of other unmeasured confounders. We cannot rule out the possibility that the associations may be due to genetic rather than environmental factors, although studies have shown that the environment exerts strong effects on prenatal and postnatal growth (24,25).
Conclusion
This study showed that components of prenatal, prepubertal, and pubertal growth have long-term effects on midlife grip strength. To the extent that these associations are modifiable, interventions in childhood that help to build muscle mass and strength, such as increased physical exercise, may have long-term beneficial effects on adult muscle strength and may help to prevent sarcopenia, disability, and frailty in later life.
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Received June 28, 2005
Accepted January 27, 2006
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