Background
Intrinsic foot muscle weakness is related to common foot pathologies and deformities [
1‐
4] and may be caused by neuromuscular conditions such as diabetic neuropathy [
5,
6] and Charcot-Marie Tooth disease [
7,
8]. Reduction in toe flexion strength is associated with an increased risk of falling in older adults [
9,
10]. The intrinsic great toe muscle abductor hallucis acts as a dynamic elevator, [
11] helps maintain balance in a medio-lateral direction [
12] and supports the medial longitudinal arch [
13]. Improving toe flexion strength can minimise the effect of foot muscle atrophy induced by disease or deformity, [
14,
15] and improve upright dynamic functional movement [
16]. The ability to reliably measure the cross-sectional area of the small first ray muscles may be an important early biomarker of treatment strategies for foot muscle weakness.
The toes are stabilised and acted on by both intrinsic and extrinsic foot muscles. Accuracy in evaluating the strength of intrinsic great toe muscles and their specific contribution to dynamic balance, or their relationship to foot morphology remains a challenge [
17]. Toe flexion force measures do not distinguish intrinsic from extrinsic foot muscles [
18]. Muscle specificity can be determined by size or cross-sectional area; however muscle size does not entirely explain differences in strength [
19]. Since the first ray performs as one functional unit, [
20] ascertaining if there is an association between the cross-sectional area of abductor hallucis (AbH) and the medial belly of flexor hallucis brevis (FHBM) muscles with measures of toe flexion force may provide a more accurate picture of the role these muscles have in medial longitudinal arch support and great toe muscle weakness.
Imaging cross-sectional area using Computerised Tomography (CT) [
21] Magnetic Resonance Imaging (MRI) [
22] or ultrasound [
23] enables analysis of specific muscles and regions of the foot. Although MRI and CT have a high level of accuracy, [
24] they are usually not immediately available in research or clinical practice due to cost. Ultrasound is a non-invasive, non-ionising and inexpensive method of assessing muscle morphology or size. Measuring cross-sectional area using ultrasound of AbH, flexor hallucis brevis, flexor digitorum brevis, quadratus plantae and abductor digiti minimus muscles in supine or prone has been reported as highly reliable [
1,
23,
25]. However, previous studies have not scanned the person in an upright position. In a clinical situation with a broad population base there can be limitations on patient’s movement ability. Some patients are unable to turn over from supine to prone or even lie down flat on a treatment table due to various problems such as: severe back problems, [
26] obesity, [
27] positional vertigo [
28] or sarcopenia [
29]. Cross-sectional area of the lower limb can also be affected by position [
30]. Therefore the scanning position was modified to determine if scanning the medial foot in seated, with the ankle in a mid-range neutral position was as reliable as the supine or prone positions. As scanning the foot on its plantar aspect was impractical with the participant seated, and on reviewing the anatomical pathways of FHB, only the medial fibres of FHB were scanned.
The aims of this study were to assess the reproducibility of assessing the size of abductor halluces (AbH) and the medial belly of flexor hallucis brevis (FHBM) muscles, and identify their relationship with toe strength, foot morphology and balance. Since the cross-sectional area and muscle thickness of the ABH, FHB, flexor digitorum brevis, quadratus plantae and lumbricals have been shown to be associated with toe flexor strength [
31] we hypothesised that a decreased size of AbH and FHBM scanned in the seated position would be similarly related to toe flexor weakness. The relationships between muscle size and foot morphology were explored as, despite the understanding that some variability in muscle thickness, [
32] size [
33] and strength [
34] may be attributed to participant characteristics, the effect of foot morphology on muscle size has yet to be determined.
Toe flexion strength has been shown to be important determinant of balance, [
35] and is related to increased single leg balance time in older adults [
36]. Correspondingly, reduced toe flexion strength has been associated with impaired balance, [
37] increased postural sway and reduced functional ability in older adults [
38]. More specifically, AbH, flexor digitorum brevis and quadratus plantae muscles increase activity with increasing postural demands and help maintain balance in a medial-lateral direction [
12]. Therefore we also hypothesised that a greater cross-sectional area of AbH and FHBM would be associated with better balance.
Results
Participants were aged 39.5 ± 10.0 years (range 26–64 yrs.); female (15/21), BMI (23.8 ± 3.3 range 19-30Kg/m
2), right foot dominant (19/21), FPI + 2.6 ± 1.5, (FPI of 2.4 ± 2.3 for adults is considered normal [
48]), with Arch height flexibility .35 mm (Table
1). Due to low body weight, one participant’s data was excluded from all pedobarographic analysis as they were unable to generate acceptable force.
Table 1
Participant characteristics of the sample (n = 21)
Participant characteristics
|
Age (y) | 39.5 ± 10.0 |
Sex, Female (%) | 15 (71%) |
Body weight (kg) | 65.5 ± 12.6 |
Height (m) | 1.65 ± 0.08 |
BMI (kg/m2) | 23.8 ± 3.3 |
Dominant foot, right | 19 (90%) |
Foot morphology
|
Foot Posture Index (− 12 to 12 score) | 2.6 ± 1.5 |
Foot length (cm) | 24.2 ± 1.3 |
Truncated foot length (cm) | 17.5 ± 0.91 |
Arch Height – sit (cm) | 6.97 ± .75 |
Arch Height – stand (cm) | 6.62 ± .74 |
Arch Height – mobility (cm) | .35 ± .17 |
Intra-rater reliability for the ultrasound measures of cross-sectional area were excellent for AbH and FHBM (Table
2). The standing paper grip test had a Kappa value of 0.203, (
p = 0.148) which is considered only slight reliability [
49].
Table 2
Reproducibility of ultrasound cross-sectional area, pedobarography, hand-held dynamometry and balance measures
Ultrasound (cm
2
)
|
CSA Abductor Hallucis | 2.16 ± 0.60 | 2.16 ± 0.63 | 0.97 | 0.94 | 0.99 |
CSA Flexor Hallucis Brevis | 1.45 ± 0.35 | 1.45 ± 0.36 | 0.96 | 0.90 | 0.98 |
Pedobarography (N)
|
Great toe press task (n = 20) | | | | | |
Stand maximum force great toe | 117.8 ± 33.8 | 128.1 ± 42.9 | 0.75 | 0.48 | 0.89 |
Hand-held dynamometry (N)
|
Stand – great toe | 124.9 ± 28.8 | 119.4 ± 28.3 | 0.75 | 0.48 | 0.89 |
Balance (cm)
|
Mean maximal step right | 89.3 ± 12.3 | 88.7 ± 12.37 | 0.83 | 0.63 | 0.93 |
Correlations between cross-sectional data are presented in Table
3. Positive significant associations were found between AbH cross-sectional area and the majority of participant characteristics (
r = .502 to
r = .625), arch height sitting (
r = .597,
p = .004), standing (
r = .590,
p = .005), toe flexion force using pedobarography (
r = 623,
p = .003) and maximum dominant step (
r = .443,
p = .044); and between FHBM cross-sectional area and foot length (
r = .451,
p = 040), truncated foot length (
r = .483,
p = .027) and FPI (
r = .544,
p = .011).
Table 3
Pearson’s correlations between ultrasound cross-sectional area and participant characteristics, foot morphology, pedobarography, hand-held dynamometry and balance measures
Participant characteristics
|
Age | 0.070 | 0.763 | −0.205 | 0.373 |
Weight | 0.662** | 0.001 | 0.305 | 0.179 |
Height | 0.559* | 0.008 | 0.372 | 0.097 |
BMI | 0.502* | 0.020 | 0.158 | 0.495 |
Foot morphology
|
Foot length | 0.582* | 0.006 | 0.451* | 0.040 |
Truncated foot length | 0.580* | 0.006 | 0.483* | 0.027 |
Foot Posture Index | 0.214 | 0.352 | 0.544* | 0.011 |
Arch height sit | 0.597** | 0.004 | 0.062 | 0.790 |
Arch height stand | 0.590** | 0.005 | 0.089 | 0.702 |
Hand-held dynamometry
|
Standing great toe force | 0.011 | 0.964 | −0.075 | 0.747 |
Pedobarography
|
Stand max force great toea | 0.645** | 0.002 | 0.349 | 0.132 |
Balance
|
Maximum step Right | 0.443* | 0.044 | 0.356 | 0.113 |
Partial correlations controlled by truncated foot length are presented in Table
4. Positive significant partial correlations, were found between AbH cross-sectional area and toe flexion force using Pedobarography (
r = 0.562,
p = .012) and between FHBM cross-sectional area and the FPI (
r = .631,
p = .003).
Table 4
Partial Pearson’s correlations (controlling for truncated foot length) between ultrasound cross-sectional area and foot morphology, pedobarography, hand-held dynamometry and balance measures
Foot morphology
|
Foot Posture Index | 0.275 | 0.240 | 0.631* | 0.003 |
Arch height sit | 0.403 | 0.078 | −0.257 | 0.274 |
Arch height stand | 0.437 | 0.054 | −0.185 | 0.436 |
Hand-held Dynamometry
|
Stand great toe forcea | 0.010 | 0.965 | −0.087 | 0.714 |
Pedobarography
|
Stand max force great toea | 0.562* | 0.012 | 0.21 | 0.389 |
Balance
|
Maximum step Right | −0.029 | 0.903 | −0.046 | 0.848 |
Discussion
We found excellent reproducibility for ultrasound cross sectional area measures of AbH and FHBM while seated. Positive significant associations were found between the cross-sectional area of AbH and the majority of participant characteristics, toe strength determined by pedobarography, foot morphology; foot length and arch height, and balance. When controlling for truncated foot length, the association with toe strength determined by pedobarography remained consistent. Associations between the cross-sectional area of FHBM were limited to one foot morphology measure.
In this study the ultrasound transducer placement and position of participant was modified from previous studies on the reliability of ultrasound cross-sectional area measures [
23,
25]. To maintain consistency of the seated ankle neutral position we scanned AbH by aligning with the navicular tubercle, this also ensured all three segments of the AbH muscle were imaged (Fig.
1a) [
50]. As well as the impracticality of scanning the plantar aspect of the foot with the participant seated, variations in FHB anatomy influenced our scanning position. The lateral head of FHB is often inseparable from the oblique head of the adductor hallucis at the insertion [
51] with difficulties in identifying the borders of FHB reported [
52]. Furthermore, an anatomical cadaveric study has shown that 20% of insertions of the oblique head of adductor hallucis attach to the navicular and align with FHB lateral fibres [
53]. Therefore, only the medial part of the FHB(M) muscle was scanned in the coronal plane on the medial-plantar aspect of the foot at about mid metatarsal in this study (Fig.
1b). This may explain the smaller cross-sectional area of FHBM from previously reported cross-sectional area FHB measures (Table
5) [
23,
25,
54]. The participant was placed in seated ankle neutral for scanning both muscles to minimise any potential positional muscle size changes [
30,
55]. The intra-rater reliability of the seated position and the scanning method of the AbH and FHBM was equivalent to previous studies [
23,
25]. The excellent reliability of this approach suggests that for people with difficulty lying supine or prone, the seated position is a good alternative to determine cross-sectional area of these foot muscles.
Table 5
Literature review of cross-sectional area values for AbH and FHB (M) by ultrasound and MRI.
| US | 2.46±0.77 | Medial hindfoot, inferior to medial malleolus | N/A | Sports active adults | |
| US | 2.75±0.34 | Medial hindfoot, inferior to medial malleolus | 2.97±0.46 | Normal foot | Plantar, proximal forefoot thickest portion |
| | 2.36±0.47 | | 2.66 ±0.46 | Pronated foot+8 | |
| US | 2.47±0.93 | Thickest portion from medial calcaneus distally towards the 1st metatarsal | N/A | Healthy adults non w/b | |
| | 2.60±0.91 | | | Weight/bearing | |
| US | 2.74± 0.64 | Medial hindfoot thickest potion between medial calcaneal tuberosity and navicular tuberosity | 2.13±0.65 | Healthy adults no HV | Plantar mid forefoot thickest portion |
| | 2.22± 0.49 | | 1.57±0.41 | Healthy adults with HV | |
| US | 2.56±0.89 | Medial hindfoot thickest portion between medial calcaneal tuberosity and navicular tuberosity | 2.45±0.53 | Healthy adults | Plantar, proximal forefoot thickest portion |
| | 2.45±0.94 | Medial hind foot inferior to medial malleolus | | | |
| US | 2.62±0.56 | Medial hindfoot, inferior to malleolus, thickest portion | Unable to determine | Runners; Normal foot | |
| | 2.74±0.39 | | | Pronated foot+ 6.6 | |
Current study | US | 2.16±0.60 | Medial, mid foot inferior to navicular tubercle thickest portion | 1.44±0.35(M) | Healthy adults | Medial-plantar mid metatarsal thickest portion |
| Muscle volume* | 6.68±2.07 | | 1.80± 0.75 FHB(M) 2.12± 0.84 FHBL | | |
| | Total CSA: FHB and AbH | |
| MRI | | 3.00 mean | | | Medial foot |
| | Total CSA : FHB, FDB, Quadratus plantae, lumbricals and AbH | |
| MRI | | 5.87±1.34 | | | Forefoot 20% of Truncated foot length |
Cross-sectional area of AbH had significant associations with the majority of participant characteristics and foot morphology. Increasing body size was related to increasing AbH size. Associations between increased arch height and increased cross-sectional area of AbH was due to anatomical dimensions as the association became non-significant when controlling for truncated foot length. Also, the majority of participants had decreased arch flexibility according to McPoil and colleagues’ dorsal arch height norms [
43]. However since arch height lowers with increased load [
56] and with plantar muscle fatigue, [
13,
57] the limited findings of the current study indicate maintenance of the height of the medial longitudinal arch may be more related to the cross-sectional area of AbH situated mid to hindfoot rather than the fore foot FHBM muscle.
In contrast, the cross-sectional area of FHBM had a substantially different pattern of association with strength, morphology and balance variables. A larger cross-sectional area of FHBM was significantly associated with a higher FPI (more pronated) even when controlled for truncated foot length. Zhang and colleagues reported a significantly larger AbH (> 4.3%) and flexor digitorum brevis (> 18.7%) associated with a more pronated FPI (6.6), [
52] (Table
5) but they did not analyse FHB due to difficulty in identifying the muscle border. They proposed that the larger forefoot muscles of people with more pronated feet contribute to control of the forefoot abduction motion during gait. Interestingly, this contrasts with Angin and colleagues study comparing normal (FPI 1.3 ± 1.2) and pronated (FPI 8.1 ± 1.7) feet [
54]. They report significantly smaller FHB (− 8.9%) and AbH (− 12%) in pronated feet compared to normal feet [
54]. These varying findings regarding associations between AbH, FHB and flexor digitorum brevis cross-sectional area and their relationships with foot type, [
52,
54] are similarly noted in studies examining intrinsic foot muscle size with age and gender, [
58,
59] foot deformity [
33,
60,
61] and plantar fasciitis [
62,
63].
Some of the results of our study contrast with previous literature reporting positive associations between measures of cross-sectional area and toe flexion force [
33,
58,
59,
64]. No association was found between cross-sectional area of either AbH or FHBM and toe flexor force measured by hand held dynamometry, which was unexpected. Previously, cross-sectional areas of intrinsic foot muscles determined by MRI were significantly correlated to measures of toe flexor strength using a toe grip dynamometer [
31,
65]. Studies reporting good reliability for toe flexion used supported dynamometers with ICCs
3,1 ranging from 0.931 [
31] to 0.97 [
2] or had participants braced or self-stabilised with ICC’s
3,1 ranging 0.81 for hallux plantar flexion [
66] to 0.95 for foot inversion [
40]. The contrasting finding in our study may be due to the technique used to complete the hand held dynamometry measures in this study [
67] (Fig.
3).
A significant association was found between cross-sectional area of AbH and great toe flexion strength measured by pedobarography. The positive relationship between increasing force and cross-sectional area was maintained even when controlling for physical dimensions, supporting previous findings [
31,
65,
68]. This suggests that the cross-sectional area of AbH may be a useful early biomarker for foot muscle weakness. In contrast, no association was found between cross-sectional area of FHBM and toe flexion force. Muscle architecture, including shape and pennation angles, reaction time, innervation, fibre type and size, influences muscle force [
69‐
72]. Ledoux [
71] reported more than double pennation in AbH, which Tosovic and colleagues suggest has three segments, with each segment acting differently due to their pennate angle and fibre type [
50,
71]. Furthermore, conflicting reports of forefoot or hindfoot muscle weakness in runners with plantar fasciitis [
3,
62,
63] and the complexity of intrinsic foot muscle weakness associated with claw toes [
60] suggests we may need to consider differentiation between fore, mid and hindfoot muscles when examining toe flexion strength related to foot problems.
Variations in muscle cross-sectional area or toe flexion force could be due to gender differences [
73] or age related sarcopenia [
50,
74]. Research to acquire the reference values for ultrasound cross-sectional area of various lower limb and foot muscles reported significant effects of age and sex on muscle thickness and echogenicity, [
32] associated with fat infiltration [
75]. We found a significant association between the size of AbH and sex, with males generally having a larger AbH, but no association between age and AbH or FHBM muscle size. Mickle and colleagues [
58] reported significant age related difference between selected intrinsic and extrinsic foot muscles. They found significant differences in toe flexion force and FHB cross-sectional area but no significant difference in AbH or flexor digitorum brevis cross-sectional area between young and older participants. Change or reduction in muscle size may also be due to stance, [
76] or loss of muscle fibres as well as decline in muscle fibre size, specifically type-II muscle fibres [
75,
77]. The difference in patterns of association between cross-sectional areas of the AbH and FHBM muscles, foot morphology and toe flexion force may be due to the small number of participants evaluated in this study, the scanning positions used, as well as the architecture of the foot.
Balance, tested via maximal step length [
45] was found to be significantly associated with AbH of the dominant leg. This suggests a positive relationship between muscle size and balance, somewhat supporting previous research, [
16] and our hypothesis that a greater cross-sectional area of AbH and FHBM would be associated with better balance. Since only the size of the AbH was positively associated with toe flexion force, it is likely that strength of the AbH muscle plays a more important role in maintaining balance than FHBM. This result is also consistent with reports of increased activity of the abductor hallucis, flexor digitorum brevis and quadratus plantae muscles during a more demanding balance task [
12]. However the relationship between AbH size and balance was not maintained after controlling for physical body size. This finding, along with the foot morphology results, highlights some associations may be entirely dependent on anthropometric variations.
There were several limitations to this study. First, only 21 healthy adults were evaluated from a sample of primarily female middle-aged adults, with less mobile or stiffer arched feet (Table
1), reducing the generalisability of the findings. Further, the small sample size resulted in a lack of statistical power with the possibility of Type 1 errors occurring as multiple comparisons were performed. Second, as this was a cross-sectional study no causality can be inferred. Third, only two muscles were measured in this study limiting comparisons with studies evaluating other intrinsic foot muscles.