1. Introduction
Compared to the characterization of the isokinetic strength of muscles operating on the shoulder and elbow joints, that of the four major muscle groups of the wrist (the flexors (F); extensors (E); and radial (R) and ulnar (U) deviators) has been very limited [
1]. This scarcity was indeed highlighted in a recent systematic review of wrist muscle strength research, which included the pronators and supinators [
2]. Among other things, this research void, especially in the clinical domain, reflects some inherent issues. For example, isokinetic dynamometers are large, nonportable and expensive instruments compared to the small isometric instruments that may be employed in hand clinics. Furthermore, the complexity of the measurement, exemplified by the multiplicity of parameters that need to be controlled, renders examination using this instrument less applicable to wrist muscles. Specifically, there is no commonly accepted protocol for isokinetic testing of the wrist or grip muscles.
Indeed, the isokinetic testing protocol of any muscle group consists of a number of critical parameters that must be maintained in order for the test findings to be interpretable. Specifically with respect to the muscles of the wrist, the main factors include the segment position, e.g., forearm in neutral vs. pronated or supinated position; body position, e.g., sitting or in standing; the range of segmental motion; the angular speed of joint motion; the speed ramping (low- vs. high-acceleration/deceleration mode); and absence or use of verbal encouragement [
1]. Furthermore, the age and sex of the participants are major confounding factors. In particular, the latter has two ramifications. First, strength findings derived from women cannot be compared with those of men. As strongly indicated with respect to the absolute isokinetic strength of the F and E, women are about 60% as strong as men [
3,
4,
5,
6,
7]. Second, combining sexes can confound interpretation, leading to non-interpretable results, as exemplified by several previous studies [
8,
9,
10,
11], and is therefore discouraged unless analyses are stratified. In addition to these hurdles, isokinetic studies of wrist muscle strength, which are based on a small number of participants [
4,
5,
6,
7,
8,
9,
10,
11], or the use of force (N) rather than moment (Nm) values, likewise preclude interpretation [
12].
Most isokinetic studies of wrist muscles focus on the F and E. In terms of sample size (N > 20) and separation of findings according to sex, six studies stand out [
3,
5,
6,
7,
13,
14]. These studies were largely limited to concentric (Con) testing, although the more recent addition of an eccentric (Ecc) component introduced a new dimension and understanding of wrist muscle action [
7,
15].
In spite of a variety of protocols, in all studies that focused on F and E, the former muscles were stronger than the latter, in both sexes alike, resulting in a maximal moment ratio: F/E of between 1.7 and 2.4. On the other hand, isokinetic assessment of the U and R muscles has been sparsely explored and based on a small number of participants [
16,
17]. Given the disparity of findings between the two papers and the omission of reference to the test range of motion (RoM) in both, the derived findings from these studies should be viewed with care. Conspicuously, only two studies included isokinetic measurements of all four muscle groups. Ağırman et al. (2017) used a mixed-sex patient group with carpal tunnel syndrome (11 women, 2 men, age range 29–60) and six healthy control subjects (4 women, 2 men, with a similar age range), to test the Con strength of all wrist muscles at 30°/s [
18]. However, due to sex pooling, very low baseline muscle strength and a wide age range, this study cannot serve as a valid source. In another study, Chu et al. (2018) [
17] followed up on the increase in wrist muscle Con strength in 9 male subjects, who had undergone targeted training, along with 10 controls. In this case, the U strength at baseline assessment was reported as significantly lower than that of the F and on par with that of the E, while post-training, against a fairly homogenous increase of around 40% in strength in the F, E and R, the gain in U strength was extraordinarily (~100%) higher. This finding was neither referred to nor explained in the text, calling into question the accuracy or the reporting of the results.
In addition, a recent study by our group revealed that by correlating the Con and Ecc strengths of the F and E, men had a significantly (
p = 0.003) higher overall inter-muscular correlation values compared to women [
7]. Whether this inter-muscle strength pattern (IMSP) is maintained upon adding the U and R could not be predicted, based on the uniqueness of this finding. Thus, extending the analysis to all four muscle groups became an additional objective.
Finally, from the clinical viewpoint, it should be noted that profiling the four wrist muscle groups in the same session allows for a fast assessment of the wrist as an integral functional unit. Therefore, the objectives of this study were threefold: (1) derive the maximal isokinetic strength profile (Con and Ecc) of the wrist F, E, U and R in healthy women and men; (2) establish a strength paradigm which depicts the inter-muscle relationships in terms of both the absolute (Nm) and bodyweight normalized (Nm/kgbw) units; (3) explore the IMSP as it applies to all four muscle groups operating on the wrist.
3. Results
None of the participants complained of inconvenience or pain during or following the tests. The mean (±SD) values of the Con and Ecc absolute and bodyweight normalized strength of the F, E, U and R, and the sex-based strength ratio of women vs. men, PM
W/PM
M (expressed in %), are outlined in
Table 1.
An independent sample t-test was conducted to examine the between-sex differences in terms of absolute and normalized strength. The results indicated that men were significantly stronger than women, by both representations, across all measured muscle groups, with the exception of the normalized Con strength of F and U. To examine the difference between the ratios, PMW/PMM (absolute and normalized), a paired samples t-test revealed that the normalized ratio (78.6 ± 8.0%) was significantly higher than the absolute’s (64.1 ± 6.6%) with a mean difference of 14.9 ± 1.1% (t[7] = 29.00, p < 0.001, Cohen’s d = 10.25).
Regarding the strength order of the four muscle groups, irrespective of contraction mode (Con or Ecc) or representation (absolute or normalized), the U was the strongest, followed successively by F, R and E, as shown by the bar graph (
Figure 3). To gain further insight into the inter-muscle relationship, the PM values of the F, E and R were expressed as a percentage of the U (
Figure 4). A three-way mixed ANOVA was conducted on the relative values, including two within-subject factors (‘muscle’ and ‘contraction mode’) and one between-subject factor (‘sex’). The analysis revealed statistically significant differences for all these main effects. Regardless of the first two factors, men demonstrated significantly higher values compared to women: 55.1% ± 9.4% vs. 47.2% ± 9.4%, respectively, F(1,38) = 7.10,
p < 0.01, η
2 = 0.156. Ecc contractions yielded significantly higher values than their Con counterparts: 53.6% ± 1.7% vs. 48.8% ± 1.4%, respectively, F(1,38) = 63.38,
p < 0.01, η
2 = 0.625. For the muscle group main factor, the F(64.8% ± 14.9%) produced significantly higher values than the R (54.6% ± 10.9%), F(1,38) = 12.50,
p < 0.001, η
2 = 0.247, which in turn were associated with significantly higher values than the E (34%.1 ± 6.2%), F(1,38) = 75.62,
p < 0.001, η
2 = 0.666.
Additionally, a significant interaction between contraction mode and muscle group was observed: F(2,76) = 26.61,
p < 0.01, η
2 = 0.412. Post hoc analyses revealed that Ecc contractions yielded significantly higher values compared to Con contractions for R (58.6% ± 11.2% vs. 50.7% ± 10.8%,
p < 0.01) and E movements (36.9% ± 6.4% vs. 31.2% ± 6.2%,
p < 0.01), while no significant difference was found for F movement (65.2% ± 10.0% vs. 64.4% ± 10.5%,
p = 0.319). Finally, sex-related differences varied as a function of muscle group and contraction mode. Men demonstrated significantly higher relative strength than women in both contraction modes for R and in Con contractions for E, while no significant sex differences were observed for F muscles across either contraction mode (
Figure 4).
Using a two-way ANOVA with repeated measures, two types of ratios were examined: (1) within ‘muscle’—between ‘contraction’, namely E/C
F, E/C
E, E/C
U and E/C
R; (2) between ‘muscle’—same ‘contraction’, namely: F/E
con, F/E
ecc, U/R
con and U/R
ecc. The values for the above ratios are outlined in
Table 2. As for the first series of ratios, the main findings revealed that the E/C
F and E/C
U were significantly higher (
p < 0.001,
p < 0.001) in men than in women, with no remarkable inter-sex differences for E/C
E and for E/C
R. Moreover, for both sexes, the E/C
U was the lowest ratio. With respect to the second series of ratios, the pairwise comparison revealed that the ratio values for men were significantly lower (
p < 0.001,
p < 0.01) in U/R
con and in U/R
ecc, compared to those of women, with no remarkable inter-sex differences for F/E
con and F/E
ecc. The analysis also revealed that in both women and men, F/E
con was significantly higher (
p < 0.001,
p < 0.001) than F/E
ecc, while U/R
con was significantly higher than U
ecc/R
ecc (
p < 0.05,
p < 0.001). Furthermore, the results show that the order of the ratio values for men and women was generally similar, with some minor differences.
Finally, the bootstrapped correlations with BCa 95% confidence intervals (presented in
Table 3 and in
Supplementary Material Table S1) indicated consistently stronger and more homogeneous associations among men compared with women. Global comparison confirmed these descriptive differences. The Jennrich’s test indicated a significant overall difference between men’s and women’s correlation matrices, χ
2(28) = 77.3,
p < 0.001. Likewise, Box’s M test supported this conclusion (M = 163.2,
p < 0.001), suggesting that the covariance structures also differ reliably between sexes. Taken together, these findings suggest that the inter-muscle strength pattern (IMSP) indices were considerably stronger and more uniform in men compared with women.
4. Discussion
This study focused on the Con and Ecc strength of the wrist muscles and their sex-related variations. The main finding is that, for both contraction types and irrespective of sex, the strongest wrist muscle group is the U, followed successively by the F, R and E. In addition, based on the inter-muscular correlations, women and men differ significantly in what may be termed as the inter-muscle strength pattern (IMSP).
The significance of the wrist muscles’ strength order lies in both the anatomical–biomechanical and the clinical domains. While the former is primarily a reflection of the force vectors of the operating muscles and their associated lever arms, the latter could provide an additional guideline in the rehabilitation of wrist injuries, especially in the presence of muscle strength deficiency. Given the particular importance of both, a preliminary assessment of the validity of the strength order is necessary. Such an assessment may be approached through three different venues. One, which is based on comparison to previous findings relating to all four muscle groups, was ruled out since the available studies could not serve this purpose for the reasons highlighted above [
17,
18]. Therefore, a more limited approach is to compare to F and E strengths, which were explored in studies that related to both sexes, employed a substantially similar test protocol, and applied the same dynamometer. Close similarity between the former and the current findings, albeit relating to only 2/4 patterns, would provide a preliminary basis for the validity of the strength order. However, prior to such a comparison, an important qualifying factor should be considered. With one exception, all past studies relating to wrist muscle strength placed the hand of the tested side in a grip configuration [
15]. This is, in fact, a direct result of the design of all wrist muscle-testing attachments serving in any of the commercially available isokinetic dynamometers, namely the use of a forearm support that provides proximal stabilization and a handle that allows a solid grip during the test. Thus, the recorded isokinetic strength reflects, at least with respect to wrist F, the cumulative effect of the actual wrist flexors as well as that of the muscles responsible for the grip.
A number of studies that quoted sex-based values and used the same angular speed (90°/s) can serve this purpose. A mean (±SD) Con PM of the F of 14.6 ± 3.4 Nm (0.26 ± 0.06 normalized) and 26.7 ± 4.5 (0.35 ± 0.04) in women and men, respectively, has been reported [
3]. The respective figures for E were 6.9 ± 1.8 (0.12 ± 0.03) and 10.5 ± 1.8 Nm (0.14 ± 0.02). In another study relating to the age decade 20–29, the PM for F in women was 10.7 ± 2.4 and 18.4 ± 3.8 in men vs. E strength of 5.7(1.4) and 9.4 ± 1.6 Nm, respectively [
3]. In a similar study of isokinetic strength in both sexes, which was spread over a wide age range, the F strength in women (N = 72) was 13.1 ± 2.8, whereas for men (N = 90) it was 22.1 ± 5.5 Nm. The respective values for E were 6.0 ± 1.7 and 11.4 ± 3.1 Nm [
6]. Finally, in a recent study which employed a slightly higher speed (120°/s) and two groups of women and men (totally different from the current study), the F strengths were 10.7 ± 2.0 Nm (0.18 ± 0.04 Nm/kgbw) and 17.9 ± 3.6 (0.24 ± 0.05) in women and men, respectively. The parallel values for E strengths were 5.84 ± 1.6 (0.10 ± 0.02) and 9.4 ± 2.5 (0.13 ± 0.03 Nm/kgbw) [
7]. Thus, except for one study whose mean values exceeded the current findings systematically by about 25%, the other reported values closely align with those derived from the present study. As for the F/E
con ratio, the present values of 2.05 ± 0.76 and 2.34 ± 0.48 in men and women, respectively, should be compared with those obtained by Forthomme et al. (2002) [
3] (2.17 ± 0.63 (men) and 2.55 ± 0.29 (women)) and Harbo et al. (2012) [
6] (1.94 and 2.2, respectively), indicating good to excellent agreement among the studies.
The second venue relates to the internal E/C ratios. When applying the same speed in maximal effort testing, the E/C ratio is >1, a physiological variant that has been reported in practically all isokinetic studies to date [
21]. In this study, all ECRs were >1, ranging from 1.04 to 1.32. Of note, the higher scores were calculated for E/C
E and E/C
R with almost perfect inter-sex similarity. For F and U, the values were lower in both sexes and significantly lower still in women compared to men. One possible explanation for this variation is the relatively higher Con vs. Ecc strength associated with the F and U muscle groups, which could possibly result from a higher exposure to concentric powerful contractions of these muscles.
The third venue relates to the inter-sex strength ratios—PM
W/PM
M. In particular, the absolute (Nm) ratios ranged from 0.57 to 0.75, with a mean value of 0.66 and 0.62 for the Con and Ecc PMs, respectively, and an overall mean of 0.64. In a recent comprehensive review that principally assessed the sex-related aspects of muscle strength and endurance, the global (all muscles) Con PM
W/PM
M ratio stood at around 0.6 [
22]. Specifically with respect to the wrist F and E, and based on the studies by Harbo et al. and others (2012), this ratio was on average 0.6 for the F and slightly smaller for the E, around 0.55 [
6]. No parallel figures were quoted for either the R or the U [
6]. In another study, the calculated values of the PM
W/PM
M ratio for Con isokinetic efforts at 30 and 90°/s and Ecc at 60°/s were 0.6, 0.55 and 0.58, respectively [
3]. The slight differences between the present findings and those derived from the abovementioned studies may also be the result of the difference between the test position of the hand, in the gravitational vs. the nongravitational planes, in the former and latter, respectively. However, probably the most valid comparison is to the findings derived from a previous study carried out by our group on a different group of same age range participants in which the only difference was in the testing speed: 120 instead of 90°/s. The absolute PM
W/PM
M ratio was 0.6 for F
con, F
ecc and E
ecc and 0.62 for E
con, and thus in excellent agreement with the current findings. The increase in the normalized (Nm/kgbw) PM
W/PM
M ratio by around 15% has been highlighted in a recent systematic review with particular reference to wrist muscles [
2]. This aligns with parallel findings relating to other muscles in the body [
23], while underlining the importance of bodyweight and sex in the predictive equation of strength (see, e.g., [
24]). In light of this finding, we recommend the parallel use of absolute and normalized isokinetic strength scores.
Hence, the collective evidence is consistent across analyses and in line with selected prior reports (especially for F/E). Moreover, in spite of the serious dearth of data relating to U and R, we suggest that the strict adherence to the protocol in all possible aspects, the relatively long inter-position break (15 min), which allowed sufficient recovery from the preceding short isokinetic efforts, and the fact that testing was completed in a single session together support the observed isokinetic strength order of the wrist muscles. Given the critical importance of the test protocol, we recommend that, for the sake of standardization, future isokinetic studies of these muscles be conducted under the same test conditions.
In trying to elucidate the underlying factor/s for the strength order, it is worth considering that ultimately, two elements take part in generating a moment around an axis: the magnitude of the force and its moment arm (MA). In biological terms, these are embodied, respectively, by the tension (in N) developed in the relevant muscle and its direction (in angular values) relative to a fixed coordinate system, and the distance (in mm) between that vector and the axis around which the 3D joint motion takes place. It is noteworthy to mention that the magnitude of the vector depends on the invariable muscle/s mass, physiological cross-sectional area (PCSA) and fiber length [
25], as well as on the level of activation, relative to the maximum, which most commonly is defined in terms of maximal isometric contraction. Thus, studies on human cadavers, which typically relate to the muscle/s’s PCSA but do not include MA data, are of limited importance in the present context [
26,
27,
28]. Of note, the data presented in these studies, which were based on diverse yet very small samples, indicated significant variations, although the PCSA and masses of U and F muscles were quite similar, with differences of 1–11%. Quite surprisingly, the PCSA and mass of the E were the highest, but without reference to the associated MAs, the strength order of the muscles could not be estimated. This was achieved in a study that tested the isometric strength of the four muscle groups using a custom-made dynamometer instrumented with a rotating load cell whose axis was aligned with the capitate bone [
29]. The mean peak isometric flexion moment was 12.2 ± 3.7 Nm, while the parallel values for E, U and R were 7.1 ± 2.1, 9.5 ± 2.2 and 11.0 ± 2.0 Nm, respectively. Thus, not only were the absolute isometric strength values much lower than those obtained in the present study, but the strength order of the muscles was different: F > R > U > E. Significantly, by estimation, F strength was greater than that of U by around 30%, whereas in the current study, U > F by more than 50%.
One possible explanation for the disparity in the findings relates to the differences in the MAs caused by a substantially different location of the center of rotation (CoR). Specifically aligning the CoR with the capitate for the isometric measurements [
29] vs. the use of the radiocarpal joint’s CoR in the present study may seriously affect the findings. Based on radiological data extracted from Indian women and men, the distance between the middle of the capitate and the radiocarpal joint is around 20 mm [
30]. Furthermore, the CoR during isokinetic motion is constantly varying, whereas in maximal isometric exertions, the CoR would be stationary once the bones are in a tight position. In addition, the test position was different: neutral (midway between pronation–supination) vs. supinatory in the present and the Delp et al. studies, respectively, which probably affected the recorded findings [
25]. Indeed, as demonstrated before in a study focusing on the estimation of the wrist joint’s CoR, the method applied for this purpose may have a massive effect on the results [
31]. As well, the models and the experimental setups have limited the analysis to the six ‘wrist only’ muscles while leaving the extrinsic muscles operating on the fingers outside the picture in spite of their role in the actions explored [
15]. However, to actually test the effect the varying MAs may have on the present results would require online imaging or noninvasive marking of the bones comprising the wrist while monitoring the tendon-associated vectors and level of activity in the muscles that operate on the wrist of live subjects during the isokinetic test. Such a task would be profoundly challenging, at the slightest, from the technical point of view. Alternatively, modeling of this system could serve this objective and shed some light on the major factors taking place in producing the moments recorded in this study. Equally, further research that is based on different isokinetic dynamometers, the same alignment axes and more diverse protocols, e.g., including isometric measurements and additional speeds, could assist in obtaining a comprehensive strength profile of the wrist muscles.
The other major finding emerging from this study indicated that men had significantly (
p = 0.003) higher overall inter-muscular correlation values compared to women. The same inter-muscle strength pattern (IMSP) was observed for the first time in a recent study conducted by our group [
7], which was limited to exploring the Con/Ecc strength of the F and E in both sexes. In the present study, this finding was expanded to include the U and R. A comprehensive literature search failed to produce a similar finding that would highlight the inter-sex differences. However, as the IMSP may reflect a higher demand for coherent muscular action, a possible explanation may be provided by a recent review, which indicated that participation in strength training was significantly higher in men than in women, with a particular emphasis on upper-body exercise [
24]. The latter could reflect on the strength of the wrist muscles, but it should be noted that the IMSP is not about the strength per se, absolute or normalized, but on the strength relationships among the muscles.
In the absence of relevant previous research, we speculate that the more pronounced IMSP in men compared to women is probably a result of the need imposed on the muscles to increase the level of muscular co-activation in order to produce higher moments about the wrist. Significantly, none of the four movement patterns is a product of a single muscle; rather, movement against resistance requires co-contraction of two or three out of the six muscles operating on the wrist, according to the following direction: for U—flexor carpi ulnaris (FCU) + extensor carpi ulnaris (ECU); for F—FCU + flexor carpi radialis (FCR); for R—FCR + extensor carpi radialis longus (ECRL) + extensor carpi radialis brevis (ECRB); and for E—ECU + ECRL + ECRB. In order to maximize the moment output, these muscles have to work together, and the higher the demand, the higher the level of co-contraction, as is well established [
32,
33]. Of note, any pair of muscles in the above has one directional movement in common and one that is opposite. For example, to produce forceful U, FCU and ECU are coactivated, but while they are agonists for U, the first is also a flexor (FCU), and the second (ECU) is an extensor. The other three movement actions demonstrate the same principle. This simultaneous agonist–antagonist action pattern, which occurs more often and at a higher intensity in men compared to women, most probably leads to the significantly higher IMSP in men. Clearly, the correct way to test this hypothesis is by using EMG or co-activation metrics, and therefore future research on the IMSP should integrate EMG and isokinetics within a single framework. Moreover, additional studies focusing on the within- and between-sex differences in IMSP relating to lower and upper extremity muscles that operate multiple planes of motion joints are needed to shed further light on this challenging relationship.
The findings of this study are qualified by three limitations. The first is a technical one: changing body position in F/E vs. U/R testing due to the need to keep the forearm in neutral position during the former’s testing is a recognized limitation. It may be solved using a special seat that is placed next to the dynamometer but which does not interfere with its action. The second relates to the actual protocol, which consisted of a single speed, short RoM, dominant side only, no gravity correction and absence of reliability estimates (ICC/CV), which could affect the generalizability of the derived findings. Attention should be given to these elements in future studies of wrist muscle strength. The third relates to the effect grip force has on the outcome measures. However, this requires an additional sensor, especially a display option, attention to which could interfere with the actual production of maximal moment output in the wrist muscles. Thus, although extrinsic finger flexors may have contributed, especially to F and U moments, we view this limitation as a relative one and recommend applying the same protocol, i.e., focusing on the production of maximal strength in the wrist muscles, without special instructions regarding the force level.