Ultrasound in Med. & Biol., Vol. 41, No. 8, pp. 2125–2130, 2015 Copyright Ó 2015 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
http://dx.doi.org/10.1016/j.ultrasmedbio.2015.04.004
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Original Contribution ASSOCIATIONS BETWEEN HANDGRIP STRENGTH AND ULTRASOUND-MEASURED MUSCLE THICKNESS OF THE HAND AND FOREARM IN YOUNG MEN AND WOMEN TAKASHI ABE, BRITTANY R. COUNTS, BRIAN E. BARNETT, SCOTT J. DANKEL, KOFAN LEE, and JEREMY P. LOENNEKE Department of Health, Exercise Science, and Recreation Management, Kevser Ermin Applied Physiology Laboratory, School of Applied Sciences, University of Mississippi, University, Mississippi, USA (Received 16 November 2014; revised 8 March 2015; in final form 6 April 2015)
Abstract—It is unknown whether muscle size of intrinsic hand muscles is associated with handgrip strength. To investigate the relationships between handgrip strength and flexor muscle size of the hand and forearm, muscle thickness (MT) of 86 young adults (43 men and 43 women) between the ages of 18 and 34 y was measured by ultrasound. Two MTs (forearm radius and forearm ulna MT) in the anterior forearm, two MTs (lumbrical and dorsal interosseous MT) in the anterior hand and handgrip strength were measured on the right side. Linear regression with part (also referred to as semipartial) correlation coefficients revealed that forearm ulna MT positively correlated with handgrip strength in both men (part 5 0.379, p 5 0.001) and women (part 5 0.268, p 5 0.002). Dorsal interosseous MT correlated with handgrip strength in women only (part 5 0.289, p 5 0.001). Our results suggest that the forearm ulna and dorsal interosseous MTs for women and forearm ulna MTs for men are factors contributing to prediction of handgrip strength in young adults. (E-mail: [email protected]) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: B-Mode ultrasound, Maximum-strength hand muscles.
INTRODUCTION
fore, alterations in skeletal muscle quantity and quality (relative strength) with age can lead to changes in handgrip strength in older adults. Handgrip strength is generated from a combination of the intrinsic and extrinsic hand muscles. The intrinsic hand muscles consist of the thenar, hypothenar and midcarpal muscles. Two major flexor muscles, the dorsal interosseous and lumbricals, are located between the metacarpals. Meanwhile, three major extrinsic flexor muscles (flexor digitorum profundus, flexor digitorum superficialis, flexor pollicis longus) are the prime movers of the digits, which are located in the anterior forearm (Drake et al. 2008). In the upper portion of the anterior forearm, two major extrinsic flexor muscles of the fingers (flexor digitorum profundus, flexor digitorum superficialis) are located near the ulna, whereas the pronator teres and brachioradialis are located near the radius. Only one study has investigated the relationships between ultrasound-measured forearm muscle thickness (MT) and handgrip strength in old men and women (Abe et al. 2014b). In that study, the MT of two muscles (forearm radius and forearm ulna MT) was measured. The authors reported that forearm ulna MT significantly
It has been reported that age-related decline in handgrip strength is associated with several unfavorable health conditions such as increased risk of functional impairment (Hairi et al. 2010; Taekema et al. 2010), morbidity (Rantanen et al. 1998) and mortality (Lauretani et al. 2003; Newman et al. 2006). Handgrip strength is the most useful criterion of age-related change in muscle strength in older adults (Cheung et al. 2012; Cruz-Jentoft et al. 2010). Age-related reduction in muscle size is a major cause of the age-related decline in muscle strength (Akagi et al. 2009). In some cases, however, the decrease in muscle strength with age is greater than what would be expected from the change in muscle mass with age (Manini and Clark 2012). There-
Address correspondence to: Takashi Abe, Department of Health, Exercise Science, and Recreation Management, The University of Mississippi, 215 Turner Center, University, MS 38677, USA. E-mail: [email protected] Conflicts of interest: The authors have no conflict of interest to declare. 2125
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correlated with handgrip strength in both men and women. However, forearm radius MT correlated with handgrip strength in women only. The reason for this apparent sex difference is unknown, but it may be related to the location and size of the major flexor muscles in the forearm (Abe et al. 2014b), as well as the contribution of intrinsic hand muscles. As described above, the forearm ulna MT includes mainly two muscles (flexor digitorum profundus, flexor digitorum superficialis), which produce flexion movement for the middle phalanges of the fingers. Interestingly, approximately 50% of handgrip strength decreased after median and ulnar nerve block compared with the pre-block measurement (Kozin et al. 1999). Therefore, it is hypothesized that handgrip strength may be associated with ultrasound-measured MT of the extrinsic as well as intrinsic muscles. The purpose of the present study was to examine the relationships between forearm and hand MT and handgrip strength.
METHODS Subjects Forty-three men and 43 women between the ages of 18 and 34 y were recruited through printed advertisement and by word of mouth from the university campus. All subjects were right-handed and free of overt chronic disease (e.g., angina, myocardial infarction, arthritic and neuromuscular disorders) and were not taking any medications known to affect muscle as assessed by self-report. The study was conducted according to the World Medical Association Declaration of Helsinki (http://www.wma. net/en/30publications/10policies/b3/index.html) and
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was approved by the university’s institutional review board. Written informed consent was obtained from all subjects before participation. Muscle thickness measurement Muscle thickness was measured using B-mode ultrasound (Aloka SSD-500, Tokyo, Japan) at two sites on the right side of the body: anterior forearm (at 30% proximal between the styloid process and the head of the radius) and anterior hand (at 55% distal between palmar digital crease and flexion crease of wrist) (Fig. 1b). After limb length measurements using anatomic landmarks described earlier, all measurement sites were marked with a marker pen and then limb girth was measured. The measurements for forearm MT were made while subjects stood quietly with the elbow extended and relaxed and the forearm supinated. Additional measurements of the right hand were made while the subjects were seated on a chair with the right hand on a table at an elbow joint angle of approximately 90 . A linear transducer with a 7.5-MHz scanning head was coated with water-soluble transmission gel to provide acoustic contact and reduce pressure by the scanning head to achieve a clear image. The scanning head was placed on the skin surface of the measurement site using the minimum pressure required, and cross sections of each muscle were imaged. Two images from each site were printed (Sony UP-897 MD, Tokyo, Japan), and mean values of each site were used for data analysis. In the lateral forearm, two MTs were measured as the perpendicular distance between the subcutaneous adipose tissue–muscle interface and muscle–bone interface of the radius (forearm radius MT) and ulna (forearm ulna MT)
Fig. 1. (a) The distance between the palmar digital crease and flexion crease of the wrist was measured to determine the measurement site. (b) Typical ultrasound image (young woman, 21 y) revealing transverse scan on the palm at 55% distal between two anatomic landmarks. DI 5 dorsal interosseous; L 5 lumbrical; MC 5 metacarpal bones.
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Table 1. Ultrasound-measured forearm and hand muscle thickness and handgrip strength in young men and women Men (n 5 43)
Age, y Height, m Body mass, kg BMI, kg/m2 Forearm girth, cm Hand girth, cm HGS, kg Muscle thickness, cm Forearm radius Forearm ulna Lumbrical Interosseous
Women (n 5 43)
Mean (SD)
Range
Mean (SD)
Range
p Value
24 (4) 1.77 (0.07) 79.8 (11.6) 25.4 (3.4) 28.1 (2.0) 22.0 (1.2) 47.3 (7.7)
20–34 1.68–1.92 54.1–101.8 16.2–34.0 21.6–33.0 18.7–25.0 33–69
23 (3) 1.62 (0.05) 64.5 (15.1) 24.4 (5.2) 24.0 (2.8) 19.2 (1.3) 25.3 (6.6)
18–33 1.48–1.72 42.9–111.4 17.2–39.0 19.3–31.5 16.0–21.6 12–38
0.267 ,0.001 ,0.001 0.294 ,0.001 ,0.001 ,0.001
2.55 (0.33) 4.31 (0.38) 0.43 (0.09) 1.10 (0.11)
2.05–3.25 3.40–5.35 0.27–0.67 0.80–1.31
1.86 (0.28) 3.46 (0.39) 0.33 (0.07) 0.87 (0.13)
1.18–2.45 2.73–4.50 0.21–0.49 0.67–1.17
,0.001 ,0.001 ,0.001 ,0.001
BMI 5 body mass index; HGS 5 handgrip strength; SD 5 standard deviation.
(Abe et al. 2014b). In the hand, MT was defined as the distance between the superficial and deep muscle fascia interfaces of the dorsal interosseous and lumbrical on the middle and ring fingers (Schweizer 2003) (Fig. 1a). The distance between the two interfaces was measured with a ruler. The precision and linearity of the image reconstruction have been confirmed and are described elsewhere (Abe et al. 2014a). Test–retest reliability of MT measurements using the intra-class correlation coefficient (ICC3,1), standard error of measurement (SEM) and minimal difference was previously determined for data from 11 young subjects (5 men and 6 women) scanned twice 24 h apart for forearm radius (0.928, 0.10 cm and 0.27 cm), forearm ulna (0.992, 0.05 cm and 0.15 cm), dorsal interosseous (0.910, 0.05 cm and 0.13 cm) and lumbrical (0.872, 0.02 cm and 0.06 cm). Handgrip strength measurement Handgrip strength was measured using a factorycalibrated hydraulic hand dynamometer (Fabrication Enterprises, Elmsford, NY, USA). All subjects were instructed to maintain an upright standing position, arms down by the side, holding the dynamometer in the right hand with the elbow flexed at 90 without squeezing the arm against the body. The size of the dynamometer’s handle was set to that with which the subjects felt comfortable while squeezing the grip. Subjects were allowed to perform one test trial, followed by two maximum trials, and the best value of the trials was used for analysis. Test–retest reliability of handgrip strength measurements using ICC3,1, SEM and minimal difference was previously determined for data from the same 11 young subjects described earlier, tested twice 24 h apart: 0.967, 2.4 kg and 6.6 kg. Statistical analysis Results are expressed as means and standard deviations for all variables. Before comparisons were made,
dependent variables were tested for normality of distribution with the Shapiro–Wilk test. Differences in the dependent variables between men and women were determined using unpaired Student t-tests. Pearson product correlations were performed to assess the relationship between handgrip strength and forearm and hand MT (single MT and summation of four MTs) and between handgrip strength and limb circumference. For men and women, linear regression was used to determine the individual relationships between four MTs of the forearm and hand and handgrip strength. Part correlation coefficients were used to determine the correlation between the MTs of the forearm and hand and handgrip strength after controlling for the influence of the remaining predictors on that predictor itself. Multicollinearity between variables was defined as a variance inflation factor $10 and/or Pearson correlations $0.85. Significance was set at p # 0.05. RESULTS Age and body mass index were similar for the sexes, although men were taller and heavier than women. Men had higher forearm and hand MT and handgrip strength than women (Table 1). Handgrip strength positively correlated with forearm radius MT (r 5 0.576 and r 5 0.732, both p , 0.001, respectively) and forearm ulna MT (r 5 0.733 and r 5 0.814, both p , 0.001, respectively) in both men and women (Fig. 2). Similarly, dorsal interosseous MT significantly correlated with handgrip strength in men (r 5 0.533, p , 0.001) and women (r 5 0.614, p , 0.001). However, there was a weak but significant correlation between handgrip strength and lumbrical MT in women (r 5 0.330, p 5 0.031), but not in men (r 5 0.191, p 5 0.221) (Fig. 3). Summation of four MTs positively correlated with handgrip strength in men (r 5 0.729, p , 0.001) and women (r 5 0.846, p , 0.001). After adjustment for three other MTs, the
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Fig. 2. Relationships between handgrip strength and forearm radius or forearm ulna MT in young men and women. MT 5 muscle thickness.
forearm ulna MT positively correlated with handgrip strength in both men and women (Table 2). Dorsal interosseous MT was correlated with handgrip strength in women only (Table 2). None of the variables met the criteria for multicollinearity (Table 2). Forearm circumference correlated with handgrip strength in men (r 5 0.623, p , 0.001) and women (r 5 0.653, p , 0.001). Hand circumference also correlated with handgrip strength in men (r 5 0.611, p , 0.001) and women (r 5 0.698, p , 0.001). DISCUSSION The intrinsic muscles of the hand would be expected to be important in hand strength and function. To the best of our knowledge, this is the first study to investigate the associations between the size of intrinsic hand muscles and handgrip strength in young adults. The primary find-
ings from the present study are that handgrip strength is moderately correlated with dorsal interosseous MT in both sexes, but lumbrical MT is correlated only in women. After adjustment for three other MTs, dorsal interosseous MT correlated with handgrip strength in women only. In the present study, dorsal interosseous and lumbrical MTs were measured at a position between metacarpal bones of the middle and ring fingers. A study reported that muscle mass and physiologic muscle crosssectional area (CSA) in the third dorsal interosseous muscle are 2.01 g and 0.95 cm2, respectively (Jacobson et al. 1992). On the other hand, physiologic CSA (0.08 cm2) in the third lumbrical is less than one-tenth that of the third dorsal interosseous. The lumbricals have the highest muscle fiber length-to-muscle length ratio in the upper extremity such that muscle fibers extended 85% to 90% of the muscle length (Jacobson et al. 1992), suggesting architectural design of this muscle may not be for force.
Fig. 3. Relationships between handgrip strength and dorsal interosseous or lumbrical MT in young men and women. MT 5 muscle thickness.
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Table 2. Linear regression with part correlation coefficients between handgrip strength and muscle thickness in the forearm and hand of young men and women Men (n 5 43)
b
Forearm radius 4.045 Forearm ulna 11.241 Dorsal interosseous 9.447 Lumbrical 25.314 0.758
Forearm radius Forearm ulna Dorsal interosseous Lumbrical
0.223 0.001 0.293 0.584 R2
R Women (n 5 43)
p Value Part CC
b
0.574
0.131 0.379 0.113 20.059 SEE
MSE
5.268 27.755
Significance ,0.001
p Value Part CC
2.035 8.046 15.706 11.316
0.557 0.002 0.001 0.172 R2
R 0.868
0.753
0.048 0.268 0.289 0.112 SEE 3.128
MSE 9.787
Significance ,0.001
Part CC 5 part correlation coefficient; MSE 5 mean squared error; SEE 5 standard error of the estimate.
In addition, lumbrical muscle has origins in the adjacent flexor digitorum profundus tendon and the peritendinous connective tissue (Jacobson et al. 1992). It is expected that if the forearm flexor muscles are strong, the lumbricals (interosseous in some cases) may not contribute to force production to a large extent during handgrip strength, which is what was observed in young men. Therefore, the results from the present study and previous study together suggest that four dorsal interosseous muscles may be a major player contributing to handgrip strength in young women. Our results support the previous findings (Abe et al. 2014b) that handgrip strength correlates strongly with forearm ulna MT in young men and women (r 5 0.733 and r 5 0.814, respectively). Forearm ulna MT includes mainly two muscles (flexor digitorum profundus, flexor digitorum superficialis), which produce flexion movement for the middle phalanges of the fingers. The total physiologic CSA of four dorsal interosseous muscles has been reported as approximately 5 cm2 (Jacobson et al. 1992). Although physiologic CSAs of the two major forearm flexor muscles to the index, middle, ring and small fingers are approximately 18 cm2 (Lieber et al. 1992), evaluating the contribution of each finger to handgrip strength is difficult. Compared with that of hand flexor muscles, the force generation capacity of forearm flexors is at least threefold higher and may be associated with handgrip strength. Therefore, forearm ulna MT may be a useful parameter predicting handgrip strength in both men and women. Abe et al. (2014b) reported that forearm radius MT correlates with handgrip strength in old women but not in old men. In the present study, a significant correlation between forearm radius MT and handgrip strength was
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observed in both young men and women. In women, the correlation coefficient between handgrip strength and forearm radius MT (r 5 0.732) was almost identical to that between handgrip strength and forearm ulna MT (r 5 0.814). In men, however, a small difference was observed in the correlation coefficient between handgrip strength and forearm ulna MT (r 5 0.733) and between handgrip strength and forearm radius MT (r 5 0.576). The difference between the previous and present studies may be associated with wider ranges of handgrip strength in young men (33–69 kg) compared with old men (25–45 kg) reported previously (Abe et al. 2014b). In addition, it is reported that decline in muscle strength in older adults is weakly associated with the loss of muscle mass (Manini and Clark 2012). Thus, compared with young adults, individual differences in muscle activation (neural factor), motor unit loss and lipid infiltration in muscle in old adults may also be associated with the differences in correlation coefficients between the two studies. Our findings indicate that forearm circumference, as well as hand circumference, is significantly correlated to handgrip strength in young men and women. Kallman et al. (1990) reported that handgrip strength is moderately related to forearm circumference (r 5 0.60) in healthy volunteers between the ages of 20 and 100 y. Abe et al. (2014b) investigated the interrelationships among forearm circumference, forearm MT and handgrip strength in old adults. They reported that forearm circumference is associated with forearm ulna MT and handgrip strength in men. In women, however, the correlation coefficient between forearm circumference and handgrip strength did not reach statistical significance (r 5 0.176, p 5 0.445) likely because of the influence of subcutaneous fat accumulation. In this study, ultrasound-measured subcutaneous adipose tissue thickness at the anterior forearm was relatively constant among men (range: 0.3–0.7 cm) and women (range: 0.4–0.9 cm). This consistency may lead to the moderate correlation coefficients observed between forearm circumference and handgrip strength in both sexes. In addition, our finding supports the previous study (Li et al. 2010) that found that hand circumference is also significantly correlated with handgrip strength in young adults. In the present study, hand circumference correlated strongly with forearm circumference in men (r 5 0.812, p , 0.001) and women (r 5 0.836, p , 0.001), suggesting concurrent muscle adaptations in the forearm and hand muscles are observed in young adults in the normal lifestyle. These muscle adaptations may be a reflection of the correlations between limb circumference and handgrip strength. A number of limitations of this study should be mentioned. First, four dorsal interosseous and four lumbrical muscles are located in the hand; we measured the MT of only the third dorsal interosseous and the third
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lumbrical. Thus, we did not compare the contributions among each of the other dorsal interosseous and lumbrical muscles. Second, the palmar interosseous muscle is also located in the hand and may contribute to handgrip strength because the palmar interosseous flexes the finger at the metacarpophalangeal joint. However, because of its small muscle volume, we did not measure the palmar interosseous (Jacobson et al. 1992). Last, it is unclear whether the association between handgrip strength and forearm/hand MT is affected by sport/physical activity or disuse in young and older adults. Additional research is needed to address these issues. CONCLUSIONS Simple correlations indicated that both hand and forearm MTs, except lumbrical MTs, are associated with handgrip strength in young men and women. After adjustment for three other MTs, only forearm ulna MT correlated positively with handgrip strength in both men and women. Hand MT (dorsal interosseous MT) correlated with handgrip strength in women only. For young adults, forearm circumference may be a viable predictor of handgrip strength. Acknowledgments—The authors thank the individuals who participated in this study. We also thank graduate students of the Department of HESRM at the University of Mississippi for their help in recruiting subjects. This study received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
REFERENCES Abe T, Loenneke JP, Thiebaud RS, Loftin M. Morphological and functional relationships with ultrasound measured muscle thickness of the upper extremity and trunk. Ultrasound 2014a;22:229–235. Abe T, Thiebaud RS, Loenneke JP, Ogawa M, Mitsukawa N. Association between forearm muscle thickness and age-related loss of skeletal muscle mass, handgrip and knee extension strength and walking performance in old men and women: A pilot study. Ultrasound Med Biol 2014b;40:2069–2075. Akagi R, Takai Y, Ohta M, Kanehisa H, Kawakami Y, Fukunaga T. Muscle volume compared to cross-sectional area is more appropriate for
Volume 41, Number 8, 2015 evaluating muscle strength in young and elderly individuals. Age Ageing 2009;38:564–569. Cheung CL, Tan KCB, Bow CH, Soong CS, Loong CH, Hung AW. Low handgrip strength is a predictor of osteoporotic fractures: Crosssectional and prospective evidence from the Hong Kong Osteoporosis Study. Age (Dordr) 2012;34:1239–1248. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M. European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis. Age Aging 2010;39:412–423. Drake RL, Vogl AW, Mitchell AW, Tibbitts RM, Richardson PE. Gray’s atlas of anatomy. Philadelphia: Churchill Livingstone Elsevier; 2008. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, Waite LM, Seibel MJ, Sambrook PN. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: The Concord Health and Ageing in Men Project. J Am Geriatr Soc 2010;58:2055–2062. Jacobson MD, Raab R, Fazeli BM, Abrams RA, Botte MJ, Lieber RL. Architectural design of the human intrinsic hand muscles. J Hand Surg Am 1992;17:804–809. Kallman DA, Plato CC, Tobin JD. The role of muscle loss in the agerelated decline of grip strength: Cross-sectional and longitudinal perspectives. J Gerontol A 1990;45:M82–M88. Kozin SH, Porter S, Clark P, Thoder JJ. The contribution of the intrinsic muscles to grip and pinch strength. J Hand Surg Am 1999;24:64–72. Lauretani F, Russo C, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L. Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia. J Appl Physiol 2003;95:1851–1860. Li K, Hewson DJ, Duchene J, Hogrel JY. Predicting maximal grip strength using hand circumference. Man Ther 2010;15:579–585. Lieber RL, Jacobson MD, Fazeli BM, Abrams RA, Botte MJ. Architecture of selected muscles of the arm and forearm: Anatomy and implications for tendon transfer. J Hand Surg Am 1992;17:787–798. Manini TM, Clark BC. Dynapenia and aging: An update. J Gerontol A Biol Sci Med Sci 2012;67A:28–40. Newman AB, Kupelian V, Visser M, Simonsick EM, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Rubin SM, Harris TB. Strength, but not muscle mass, is associated with mortality in the Health, Aging and Body Composition Study Cohort. J Gerontol A Biol Sci Med Sci 2006;61A:72–77. Rantanen T, Masaki K, Foley D, Izmirlian G, White L, Guralnik JM. Grip strength over 27 yr in Japanese-American men. J Appl Physiol 1998;85:2047–2053. Schweizer A. Lumbrical tears in rock climbers. J Hand Surg Br 2003;28: 187–189. Taekema DG, Gussekloo J, Maier AB, Westendorp RG, de Craen AJ. Handgrip strength as a predictor of functional, psychological and social health: A prospective population-based study among the oldest old. Age Aging 2010;39:331–337.
http://dx.doi.org/10.1016/j.ultrasmedbio.2015.04.004
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Original Contribution ASSOCIATIONS BETWEEN HANDGRIP STRENGTH AND ULTRASOUND-MEASURED MUSCLE THICKNESS OF THE HAND AND FOREARM IN YOUNG MEN AND WOMEN TAKASHI ABE, BRITTANY R. COUNTS, BRIAN E. BARNETT, SCOTT J. DANKEL, KOFAN LEE, and JEREMY P. LOENNEKE Department of Health, Exercise Science, and Recreation Management, Kevser Ermin Applied Physiology Laboratory, School of Applied Sciences, University of Mississippi, University, Mississippi, USA (Received 16 November 2014; revised 8 March 2015; in final form 6 April 2015)
Abstract—It is unknown whether muscle size of intrinsic hand muscles is associated with handgrip strength. To investigate the relationships between handgrip strength and flexor muscle size of the hand and forearm, muscle thickness (MT) of 86 young adults (43 men and 43 women) between the ages of 18 and 34 y was measured by ultrasound. Two MTs (forearm radius and forearm ulna MT) in the anterior forearm, two MTs (lumbrical and dorsal interosseous MT) in the anterior hand and handgrip strength were measured on the right side. Linear regression with part (also referred to as semipartial) correlation coefficients revealed that forearm ulna MT positively correlated with handgrip strength in both men (part 5 0.379, p 5 0.001) and women (part 5 0.268, p 5 0.002). Dorsal interosseous MT correlated with handgrip strength in women only (part 5 0.289, p 5 0.001). Our results suggest that the forearm ulna and dorsal interosseous MTs for women and forearm ulna MTs for men are factors contributing to prediction of handgrip strength in young adults. (E-mail: [email protected]) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: B-Mode ultrasound, Maximum-strength hand muscles.
INTRODUCTION
fore, alterations in skeletal muscle quantity and quality (relative strength) with age can lead to changes in handgrip strength in older adults. Handgrip strength is generated from a combination of the intrinsic and extrinsic hand muscles. The intrinsic hand muscles consist of the thenar, hypothenar and midcarpal muscles. Two major flexor muscles, the dorsal interosseous and lumbricals, are located between the metacarpals. Meanwhile, three major extrinsic flexor muscles (flexor digitorum profundus, flexor digitorum superficialis, flexor pollicis longus) are the prime movers of the digits, which are located in the anterior forearm (Drake et al. 2008). In the upper portion of the anterior forearm, two major extrinsic flexor muscles of the fingers (flexor digitorum profundus, flexor digitorum superficialis) are located near the ulna, whereas the pronator teres and brachioradialis are located near the radius. Only one study has investigated the relationships between ultrasound-measured forearm muscle thickness (MT) and handgrip strength in old men and women (Abe et al. 2014b). In that study, the MT of two muscles (forearm radius and forearm ulna MT) was measured. The authors reported that forearm ulna MT significantly
It has been reported that age-related decline in handgrip strength is associated with several unfavorable health conditions such as increased risk of functional impairment (Hairi et al. 2010; Taekema et al. 2010), morbidity (Rantanen et al. 1998) and mortality (Lauretani et al. 2003; Newman et al. 2006). Handgrip strength is the most useful criterion of age-related change in muscle strength in older adults (Cheung et al. 2012; Cruz-Jentoft et al. 2010). Age-related reduction in muscle size is a major cause of the age-related decline in muscle strength (Akagi et al. 2009). In some cases, however, the decrease in muscle strength with age is greater than what would be expected from the change in muscle mass with age (Manini and Clark 2012). There-
Address correspondence to: Takashi Abe, Department of Health, Exercise Science, and Recreation Management, The University of Mississippi, 215 Turner Center, University, MS 38677, USA. E-mail: [email protected] Conflicts of interest: The authors have no conflict of interest to declare. 2125
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correlated with handgrip strength in both men and women. However, forearm radius MT correlated with handgrip strength in women only. The reason for this apparent sex difference is unknown, but it may be related to the location and size of the major flexor muscles in the forearm (Abe et al. 2014b), as well as the contribution of intrinsic hand muscles. As described above, the forearm ulna MT includes mainly two muscles (flexor digitorum profundus, flexor digitorum superficialis), which produce flexion movement for the middle phalanges of the fingers. Interestingly, approximately 50% of handgrip strength decreased after median and ulnar nerve block compared with the pre-block measurement (Kozin et al. 1999). Therefore, it is hypothesized that handgrip strength may be associated with ultrasound-measured MT of the extrinsic as well as intrinsic muscles. The purpose of the present study was to examine the relationships between forearm and hand MT and handgrip strength.
METHODS Subjects Forty-three men and 43 women between the ages of 18 and 34 y were recruited through printed advertisement and by word of mouth from the university campus. All subjects were right-handed and free of overt chronic disease (e.g., angina, myocardial infarction, arthritic and neuromuscular disorders) and were not taking any medications known to affect muscle as assessed by self-report. The study was conducted according to the World Medical Association Declaration of Helsinki (http://www.wma. net/en/30publications/10policies/b3/index.html) and
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was approved by the university’s institutional review board. Written informed consent was obtained from all subjects before participation. Muscle thickness measurement Muscle thickness was measured using B-mode ultrasound (Aloka SSD-500, Tokyo, Japan) at two sites on the right side of the body: anterior forearm (at 30% proximal between the styloid process and the head of the radius) and anterior hand (at 55% distal between palmar digital crease and flexion crease of wrist) (Fig. 1b). After limb length measurements using anatomic landmarks described earlier, all measurement sites were marked with a marker pen and then limb girth was measured. The measurements for forearm MT were made while subjects stood quietly with the elbow extended and relaxed and the forearm supinated. Additional measurements of the right hand were made while the subjects were seated on a chair with the right hand on a table at an elbow joint angle of approximately 90 . A linear transducer with a 7.5-MHz scanning head was coated with water-soluble transmission gel to provide acoustic contact and reduce pressure by the scanning head to achieve a clear image. The scanning head was placed on the skin surface of the measurement site using the minimum pressure required, and cross sections of each muscle were imaged. Two images from each site were printed (Sony UP-897 MD, Tokyo, Japan), and mean values of each site were used for data analysis. In the lateral forearm, two MTs were measured as the perpendicular distance between the subcutaneous adipose tissue–muscle interface and muscle–bone interface of the radius (forearm radius MT) and ulna (forearm ulna MT)
Fig. 1. (a) The distance between the palmar digital crease and flexion crease of the wrist was measured to determine the measurement site. (b) Typical ultrasound image (young woman, 21 y) revealing transverse scan on the palm at 55% distal between two anatomic landmarks. DI 5 dorsal interosseous; L 5 lumbrical; MC 5 metacarpal bones.
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Table 1. Ultrasound-measured forearm and hand muscle thickness and handgrip strength in young men and women Men (n 5 43)
Age, y Height, m Body mass, kg BMI, kg/m2 Forearm girth, cm Hand girth, cm HGS, kg Muscle thickness, cm Forearm radius Forearm ulna Lumbrical Interosseous
Women (n 5 43)
Mean (SD)
Range
Mean (SD)
Range
p Value
24 (4) 1.77 (0.07) 79.8 (11.6) 25.4 (3.4) 28.1 (2.0) 22.0 (1.2) 47.3 (7.7)
20–34 1.68–1.92 54.1–101.8 16.2–34.0 21.6–33.0 18.7–25.0 33–69
23 (3) 1.62 (0.05) 64.5 (15.1) 24.4 (5.2) 24.0 (2.8) 19.2 (1.3) 25.3 (6.6)
18–33 1.48–1.72 42.9–111.4 17.2–39.0 19.3–31.5 16.0–21.6 12–38
0.267 ,0.001 ,0.001 0.294 ,0.001 ,0.001 ,0.001
2.55 (0.33) 4.31 (0.38) 0.43 (0.09) 1.10 (0.11)
2.05–3.25 3.40–5.35 0.27–0.67 0.80–1.31
1.86 (0.28) 3.46 (0.39) 0.33 (0.07) 0.87 (0.13)
1.18–2.45 2.73–4.50 0.21–0.49 0.67–1.17
,0.001 ,0.001 ,0.001 ,0.001
BMI 5 body mass index; HGS 5 handgrip strength; SD 5 standard deviation.
(Abe et al. 2014b). In the hand, MT was defined as the distance between the superficial and deep muscle fascia interfaces of the dorsal interosseous and lumbrical on the middle and ring fingers (Schweizer 2003) (Fig. 1a). The distance between the two interfaces was measured with a ruler. The precision and linearity of the image reconstruction have been confirmed and are described elsewhere (Abe et al. 2014a). Test–retest reliability of MT measurements using the intra-class correlation coefficient (ICC3,1), standard error of measurement (SEM) and minimal difference was previously determined for data from 11 young subjects (5 men and 6 women) scanned twice 24 h apart for forearm radius (0.928, 0.10 cm and 0.27 cm), forearm ulna (0.992, 0.05 cm and 0.15 cm), dorsal interosseous (0.910, 0.05 cm and 0.13 cm) and lumbrical (0.872, 0.02 cm and 0.06 cm). Handgrip strength measurement Handgrip strength was measured using a factorycalibrated hydraulic hand dynamometer (Fabrication Enterprises, Elmsford, NY, USA). All subjects were instructed to maintain an upright standing position, arms down by the side, holding the dynamometer in the right hand with the elbow flexed at 90 without squeezing the arm against the body. The size of the dynamometer’s handle was set to that with which the subjects felt comfortable while squeezing the grip. Subjects were allowed to perform one test trial, followed by two maximum trials, and the best value of the trials was used for analysis. Test–retest reliability of handgrip strength measurements using ICC3,1, SEM and minimal difference was previously determined for data from the same 11 young subjects described earlier, tested twice 24 h apart: 0.967, 2.4 kg and 6.6 kg. Statistical analysis Results are expressed as means and standard deviations for all variables. Before comparisons were made,
dependent variables were tested for normality of distribution with the Shapiro–Wilk test. Differences in the dependent variables between men and women were determined using unpaired Student t-tests. Pearson product correlations were performed to assess the relationship between handgrip strength and forearm and hand MT (single MT and summation of four MTs) and between handgrip strength and limb circumference. For men and women, linear regression was used to determine the individual relationships between four MTs of the forearm and hand and handgrip strength. Part correlation coefficients were used to determine the correlation between the MTs of the forearm and hand and handgrip strength after controlling for the influence of the remaining predictors on that predictor itself. Multicollinearity between variables was defined as a variance inflation factor $10 and/or Pearson correlations $0.85. Significance was set at p # 0.05. RESULTS Age and body mass index were similar for the sexes, although men were taller and heavier than women. Men had higher forearm and hand MT and handgrip strength than women (Table 1). Handgrip strength positively correlated with forearm radius MT (r 5 0.576 and r 5 0.732, both p , 0.001, respectively) and forearm ulna MT (r 5 0.733 and r 5 0.814, both p , 0.001, respectively) in both men and women (Fig. 2). Similarly, dorsal interosseous MT significantly correlated with handgrip strength in men (r 5 0.533, p , 0.001) and women (r 5 0.614, p , 0.001). However, there was a weak but significant correlation between handgrip strength and lumbrical MT in women (r 5 0.330, p 5 0.031), but not in men (r 5 0.191, p 5 0.221) (Fig. 3). Summation of four MTs positively correlated with handgrip strength in men (r 5 0.729, p , 0.001) and women (r 5 0.846, p , 0.001). After adjustment for three other MTs, the
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Fig. 2. Relationships between handgrip strength and forearm radius or forearm ulna MT in young men and women. MT 5 muscle thickness.
forearm ulna MT positively correlated with handgrip strength in both men and women (Table 2). Dorsal interosseous MT was correlated with handgrip strength in women only (Table 2). None of the variables met the criteria for multicollinearity (Table 2). Forearm circumference correlated with handgrip strength in men (r 5 0.623, p , 0.001) and women (r 5 0.653, p , 0.001). Hand circumference also correlated with handgrip strength in men (r 5 0.611, p , 0.001) and women (r 5 0.698, p , 0.001). DISCUSSION The intrinsic muscles of the hand would be expected to be important in hand strength and function. To the best of our knowledge, this is the first study to investigate the associations between the size of intrinsic hand muscles and handgrip strength in young adults. The primary find-
ings from the present study are that handgrip strength is moderately correlated with dorsal interosseous MT in both sexes, but lumbrical MT is correlated only in women. After adjustment for three other MTs, dorsal interosseous MT correlated with handgrip strength in women only. In the present study, dorsal interosseous and lumbrical MTs were measured at a position between metacarpal bones of the middle and ring fingers. A study reported that muscle mass and physiologic muscle crosssectional area (CSA) in the third dorsal interosseous muscle are 2.01 g and 0.95 cm2, respectively (Jacobson et al. 1992). On the other hand, physiologic CSA (0.08 cm2) in the third lumbrical is less than one-tenth that of the third dorsal interosseous. The lumbricals have the highest muscle fiber length-to-muscle length ratio in the upper extremity such that muscle fibers extended 85% to 90% of the muscle length (Jacobson et al. 1992), suggesting architectural design of this muscle may not be for force.
Fig. 3. Relationships between handgrip strength and dorsal interosseous or lumbrical MT in young men and women. MT 5 muscle thickness.
Handgrip strength and US-measured muscle thickness d T. ABE et al.
Table 2. Linear regression with part correlation coefficients between handgrip strength and muscle thickness in the forearm and hand of young men and women Men (n 5 43)
b
Forearm radius 4.045 Forearm ulna 11.241 Dorsal interosseous 9.447 Lumbrical 25.314 0.758
Forearm radius Forearm ulna Dorsal interosseous Lumbrical
0.223 0.001 0.293 0.584 R2
R Women (n 5 43)
p Value Part CC
b
0.574
0.131 0.379 0.113 20.059 SEE
MSE
5.268 27.755
Significance ,0.001
p Value Part CC
2.035 8.046 15.706 11.316
0.557 0.002 0.001 0.172 R2
R 0.868
0.753
0.048 0.268 0.289 0.112 SEE 3.128
MSE 9.787
Significance ,0.001
Part CC 5 part correlation coefficient; MSE 5 mean squared error; SEE 5 standard error of the estimate.
In addition, lumbrical muscle has origins in the adjacent flexor digitorum profundus tendon and the peritendinous connective tissue (Jacobson et al. 1992). It is expected that if the forearm flexor muscles are strong, the lumbricals (interosseous in some cases) may not contribute to force production to a large extent during handgrip strength, which is what was observed in young men. Therefore, the results from the present study and previous study together suggest that four dorsal interosseous muscles may be a major player contributing to handgrip strength in young women. Our results support the previous findings (Abe et al. 2014b) that handgrip strength correlates strongly with forearm ulna MT in young men and women (r 5 0.733 and r 5 0.814, respectively). Forearm ulna MT includes mainly two muscles (flexor digitorum profundus, flexor digitorum superficialis), which produce flexion movement for the middle phalanges of the fingers. The total physiologic CSA of four dorsal interosseous muscles has been reported as approximately 5 cm2 (Jacobson et al. 1992). Although physiologic CSAs of the two major forearm flexor muscles to the index, middle, ring and small fingers are approximately 18 cm2 (Lieber et al. 1992), evaluating the contribution of each finger to handgrip strength is difficult. Compared with that of hand flexor muscles, the force generation capacity of forearm flexors is at least threefold higher and may be associated with handgrip strength. Therefore, forearm ulna MT may be a useful parameter predicting handgrip strength in both men and women. Abe et al. (2014b) reported that forearm radius MT correlates with handgrip strength in old women but not in old men. In the present study, a significant correlation between forearm radius MT and handgrip strength was
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observed in both young men and women. In women, the correlation coefficient between handgrip strength and forearm radius MT (r 5 0.732) was almost identical to that between handgrip strength and forearm ulna MT (r 5 0.814). In men, however, a small difference was observed in the correlation coefficient between handgrip strength and forearm ulna MT (r 5 0.733) and between handgrip strength and forearm radius MT (r 5 0.576). The difference between the previous and present studies may be associated with wider ranges of handgrip strength in young men (33–69 kg) compared with old men (25–45 kg) reported previously (Abe et al. 2014b). In addition, it is reported that decline in muscle strength in older adults is weakly associated with the loss of muscle mass (Manini and Clark 2012). Thus, compared with young adults, individual differences in muscle activation (neural factor), motor unit loss and lipid infiltration in muscle in old adults may also be associated with the differences in correlation coefficients between the two studies. Our findings indicate that forearm circumference, as well as hand circumference, is significantly correlated to handgrip strength in young men and women. Kallman et al. (1990) reported that handgrip strength is moderately related to forearm circumference (r 5 0.60) in healthy volunteers between the ages of 20 and 100 y. Abe et al. (2014b) investigated the interrelationships among forearm circumference, forearm MT and handgrip strength in old adults. They reported that forearm circumference is associated with forearm ulna MT and handgrip strength in men. In women, however, the correlation coefficient between forearm circumference and handgrip strength did not reach statistical significance (r 5 0.176, p 5 0.445) likely because of the influence of subcutaneous fat accumulation. In this study, ultrasound-measured subcutaneous adipose tissue thickness at the anterior forearm was relatively constant among men (range: 0.3–0.7 cm) and women (range: 0.4–0.9 cm). This consistency may lead to the moderate correlation coefficients observed between forearm circumference and handgrip strength in both sexes. In addition, our finding supports the previous study (Li et al. 2010) that found that hand circumference is also significantly correlated with handgrip strength in young adults. In the present study, hand circumference correlated strongly with forearm circumference in men (r 5 0.812, p , 0.001) and women (r 5 0.836, p , 0.001), suggesting concurrent muscle adaptations in the forearm and hand muscles are observed in young adults in the normal lifestyle. These muscle adaptations may be a reflection of the correlations between limb circumference and handgrip strength. A number of limitations of this study should be mentioned. First, four dorsal interosseous and four lumbrical muscles are located in the hand; we measured the MT of only the third dorsal interosseous and the third
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lumbrical. Thus, we did not compare the contributions among each of the other dorsal interosseous and lumbrical muscles. Second, the palmar interosseous muscle is also located in the hand and may contribute to handgrip strength because the palmar interosseous flexes the finger at the metacarpophalangeal joint. However, because of its small muscle volume, we did not measure the palmar interosseous (Jacobson et al. 1992). Last, it is unclear whether the association between handgrip strength and forearm/hand MT is affected by sport/physical activity or disuse in young and older adults. Additional research is needed to address these issues. CONCLUSIONS Simple correlations indicated that both hand and forearm MTs, except lumbrical MTs, are associated with handgrip strength in young men and women. After adjustment for three other MTs, only forearm ulna MT correlated positively with handgrip strength in both men and women. Hand MT (dorsal interosseous MT) correlated with handgrip strength in women only. For young adults, forearm circumference may be a viable predictor of handgrip strength. Acknowledgments—The authors thank the individuals who participated in this study. We also thank graduate students of the Department of HESRM at the University of Mississippi for their help in recruiting subjects. This study received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
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