Importance and challenges of measuring intrinsic foot muscle strength

Background:Intrinsic foot muscle weakness has been implicated in a range of foot deformities and disorders. However, to establish a relationship between intrinsic muscle weakness and foot pathology, an objective measure of intrinsic muscle strength is needed. The aim of this review was to provide an overview of the anatomy and role of intrinsic foot muscles, implications of intrinsic weakness and evaluate the different methods used to measure intrinsic foot muscle strength. Method:Literature was sourced from database searches of MEDLINE, PubMed, SCOPUS, Cochrane Library, PEDro and CINAHL up to June 2012. Results:There is no widely accepted method of measuring intrinsic foot muscle strength. Methods to estimate toe flexor muscle strength include the paper grip test, plantar pressure, toe dynamometry, and the intrinsic positive test. Hand-held dynamometry has excellent interrater and intrarater reliability and limits toe curling, which is an action hypothesised to activate extrinsic toe flexor muscles. However, it is unclear whether any method can actually isolate intrinsic muscle strength. Also most methods measure only toe flexor strength and other actions such as toe extension and abduction have not been adequately assessed. Indirect methods to investigate intrinsic muscle structure and performance include CT, ultrasonography, MRI, EMG, and muscle biopsy. Indirect methods often discriminate between intrinsic and extrinsic muscles, but lack the ability to measure muscle force. Conclusions:There are many challenges to accurately measure intrinsic muscle strength in isolation. Most studies have measured toe flexor strength as a surrogate measure of intrinsic muscle strength. Hand-held dynamometry appears to be a promising method of estimating intrinsic muscle strength. However, the contribution of extrinsic muscles cannot be excluded from toe flexor strength measurement. Future research should clarify the relative contribution of intrinsic and extrinsic muscles during intrinsic foot muscle strength testing. Keywords:Foot, Muscles, Toes, Muscle strength, Dynamometer Introduction Intrinsic foot muscles contribute to the support of the medial longitudinal arch [1,2] and are thought to work in conjunction with the plantar aponeurosis, plantar ligaments and extrinsic

be excluded from toe flexor strength measurement. Future research should clarify the relative contribution of intrinsic and extrinsic muscles during intrinsic foot muscle strength testing. Keywords:Foot, Muscles, Toes, Muscle strength, Dynamometer Introduction Intrinsic foot muscles contribute to the support of the medial longitudinal arch [1,2] and are thought to work in conjunction with the plantar aponeurosis, plantar ligaments and extrinsic foot muscles to control the stres- ses on the foot during gait [3-5]. Intrinsic foot muscle weakness has also been implicated in the development of pes cavus in Charcot-Marie-Tooth disease (CMT) [6,7], heel pain [1,8,9], claw toe deformity [10], hammer toe deformity [10,11], and hallux valgus [10,12,13]. The level of intrinsic muscle weakness necessary for the development of these deformities and disorders is un- known. To assess the degree of weakness and to deter- mine the effect of strengthening intrinsic muscles, a valid and reliable measure of intrinsic muscle strength is needed. There are diverse methods available for measur- ing intrinsic muscle properties [3,12-24], but there is lack of agreement regarding the most appropriate meas- ure of strength. Therefore, the aim of this review was to provide an overview of the anatomy and role of intrinsic foot muscles, implications of intrinsic weakness and evaluate the different methods used to measure intrinsic foot muscle strength. * Correspondence:achini.d.soysa@gmail.com 1 Arthritis & Musculoskeletal Research Group, Faculty of Health Science, University of Sydney, Sydney, Australia Full list of author information is available at the end of the article JOURNAL OF FOOT AND ANKLE RESEARCH © 2012 Soysa et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Soysaet al. Journal of Foot and Ankle Research2012,5:29 http://www.jfootankleres.com/content/5/1/29

Method The electronic databases MEDLINE, PubMed, SCOPUS, Cochrane Library and CINAHL were searched between 21 May and 21 June 2012 to locate scientific articles on intrinsic foot muscles and muscle strength measure- ment. The main search terms and number of articles retrieved are listed in Table 1, 2, 3, 4 and 5. The search engine PEDro was also accessed and one article [25] was retrieved in the search results. Further articles were identified by hand searching reference lists of the extracted articles. Google Scholar was also searched to identify any relevant unpublished or in press articles using the same search terms as those used in the data- base searches. The abstracts of the located articles were then read to select the appropriate articles, with full cop- ies of the articles examined if the study was relevant to the research aim. Fifty three research articles were identified that related to intrinsic foot muscles and strength measurement. Articles had to meet certain criteria for inclusion. The inclusion criteria were as follows. (i) Research related to the role of intrinsic foot muscles (ii) Research related to the anatomy of intrinsic foot muscles (iii)Research describing the measurement of intrinsic muscles and toe muscle strength or weakness. Papers relating to the intrinsic foot muscle strength were considered initially, but it became apparent that few papers existed. Therefore the search was broadened to include articles relating to the measurement of toe muscles (iv)Publication in peer-reviewed journals (v) Full-text English language articles Anatomy of the intrinsic foot muscles The plantar and dorsal intrinsic muscles of the foot have both their origin and insertion within the foot [26,27]. Intrinsic foot muscles differ from extrinsic foot muscles, which have their origins in the leg and the long tendons cross the ankle joint complex [27]. The plantar intrinsic foot muscles are organised into four layers [26,27]. The most superficial layer is deep to theplantar aponeurosis and includes theabductor hallucis, flexor digitorum brevis, and theabductor digiti minimi[26]. The second layer consists of thequadratus plantaeandthe lumbricals.The third layer consists ofadductor hallucis transverse, adductor hallucis oblique,flexor hallucis brevisandflexor digiti minimi brevis. The deepest

the ankle joint complex [27]. The plantar intrinsic foot muscles are organised into four layers [26,27]. The most superficial layer is deep to theplantar aponeurosis and includes theabductor hallucis, flexor digitorum brevis, and theabductor digiti minimi[26]. The second layer consists of thequadratus plantaeandthe lumbricals.The third layer consists ofadductor hallucis transverse, adductor hallucis oblique,flexor hallucis brevisandflexor digiti minimi brevis. The deepest layer consists of the threeplantar interossei. All the plantar intrinsic muscles are innervated by the medial and lateral plantar branches of the tibial nerve [27]. The dorsal intrinsic muscles of the foot can be divided into two layers [26]. The most superficial layer consists of theextensor hallucis brevisandextensor digitorum brevis. The deep layer consists of thedorsal interossei muscles. Theextensor hallucis brevisandextensor digi- torum brevisis innervated by the deep fibular nerve while thedorsal interosseiare innervated by the lateral plantar nerve with the first and seconddorsal interossei also receiving part of their innervation from the deep fibular nerve [27]. The dorsal intrinsic muscles have rarely been described in the scientific literature and their function in the foot remains largely unknown [28]. Early EMG studies revealed that the recruitment pattern of theextensor hallucis brevisandextensor digitorum brevis Table 1 Database search strategy for PubMed Number Search terms Results* 1. foot 95709 2. muscle 813998 3. intrinsic 96812 4. Number 1+2+3 260 5. measure 487905 6. strength 166587 7. Number 1+2+3+5 18 8. Number 1+2+3+6 28 *The results are from the search conducted on the electronic database PubMed between May and June 2012. Table 2 Database search strategy for MEDLINE Number Search terms Results* 1. foot 43149 2. muscle 297428 3. intrinsic 59556 4. Number 1+2+3 113 5. measure 21182 6. strength 110271 7. Number 1+2+3+5 3 8. Number 1+2+3+6 18 *The results are from the search conducted on the electronic database MEDLINE between May and June 2012. Table 3 Database search strategy for EBSCO/CINAHL Number Search terms Results* 1. foot 21242 2. muscle 55954 3. intrinsic 4084 4. Number 1+2+3 44 5. measure 52005 6. strength 28651 7. Number 1+2+3+5 2 8. Number 1+2+3+6 12 *The results are from the search conducted on the

the search conducted on the electronic database MEDLINE between May and June 2012. Table 3 Database search strategy for EBSCO/CINAHL Number Search terms Results* 1. foot 21242 2. muscle 55954 3. intrinsic 4084 4. Number 1+2+3 44 5. measure 52005 6. strength 28651 7. Number 1+2+3+5 2 8. Number 1+2+3+6 12 *The results are from the search conducted on the electronic database EBSCO/ CINAHL between May and June 2012. Soysaet al. Journal of Foot and Ankle Research2012,5:29 Page 2 of 14 http://www.jfootankleres.com/content/5/1/29

during walking varied significantly between participants, with some participants demonstrating no activation of extensor digitorum brevisduring gait [29].Theextensor hallucis brevisandextensor digitorum brevismuscles are now widely used in tissue grafts, such as the island flap to cover soft tissue defects in the distal leg and ankle regions [30]. Therefore, very little is known about the specific roles of dorsal intrinsic muscles and will not be further discussed in this review. Evolution of the intrinsic foot muscles It has been hypothesised that during human evolution, toe flexor force and function are gradually diminishing and therefore plantar intrinsic muscles are becoming largely redundant in the foot [31]. In simian primates, toes are longer and have specialised functions, with toes used to climb trees [32]. Conversely humans have shorter phalanges, which may be a morphological adap- tation to the reduced prehensile use of toes in shod wearing modern humans [31]. This theory of adaptive changes during human evolution is supported by the findings of a 3.6 million year old partial human foot, where the toes were shorter than the African ape but longer and more curved than the modern human foot [33]. Some authors have suggested that continued func- tion of some intrinsic muscles may reflect incomplete evolutionary processes [12]. However, the existence of muscles like thequadratus plantaedisproves this hy- pothesis. The medial and lateral attachment sites of the quadratus plantaemuscle into the calcaneus is unique to humans [34] andquadratus plantaeis unique to the foot as there is no analogous muscle in the hand [34]. Since theflexor digitorum longustendon enters the foot from the medial side and pulls the toes medially [35], one theory suggests that the concurrent contraction of the quadratus plantaeallows the toes to flex in the sagittal plane by redirecting the pull of theflexor digitorum longus.This is a necessary development for bipedal ambulation [35]. Therefore, the existence of specialised functions for intrinsic muscles, may suggest that intrinsic foot muscles continue to have a role in the modern foot. Role of intrinsic foot muscles Walking A number of studies reveal that intrinsic foot muscles are active as a group during walking [3,4,36].

pull of theflexor digitorum longus.This is a necessary development for bipedal ambulation [35]. Therefore, the existence of specialised functions for intrinsic muscles, may suggest that intrinsic foot muscles continue to have a role in the modern foot. Role of intrinsic foot muscles Walking A number of studies reveal that intrinsic foot muscles are active as a group during walking [3,4,36]. A classic electromyography (EMG) study of 12 participants showed thatabductor digiti minimi, abductor hallucis, flexor digitorum brevis,dorsal interossei and lumbrical muscles were all active during the stance phase of gait and continued until toe off [3]. A study by Jacob 2001 combined anthropometrical and plantar pressure data to reveal thatflexor hallucis brevis(in combination with abductor hallucis) andflexor digitorum brevismuscles are able to exert forces approximately 36% and 13% of body weight during the propulsive phase of walking [37]. However, it is unknown whether these muscles act con- centrically or eccentrically [31] or have other actions in- cluding toe abduction [38]. Mann and Inman [3] suggested that the role of the intrinsic foot muscles is stabilisation of the foot during propulsion. Intrinsic muscle activity during the propulsion phase of gait coin- cides with passive metatarsophalangeal (MTP) joint dorsiflexion, as the centre of mass moves anterior to the metatarsophalangeal joint. Rolianet al.[31] and Gold- mann and Bruggemann [39] postulated that the role of the intrinsic and extrinsic toe flexor muscles is to coun- terbalance the dorsiflexion moment of the ground reac- tion force at the metatarsophalangeal joint, in the push off phase of walking. This may be achieved by eccentric contraction of the long and short toe flexor muscles to control dorsiflexion at the MTP joint and maintain interphalangeal joint extension, to enable flat toes on the ground until toe off [32,40]. Therefore, by increasing the surface area in contact with the ground, this would im- prove pressure distribution under the metatarsal heads during walking. Arch support The role of intrinsic muscles in the support of the med- ial longitudinal arch has been investigated in both stand- ing [3-5] and walking [4,9]. Early EMG studies revealed that intrinsic foot muscles are not

Therefore, by increasing the surface area in contact with the ground, this would im- prove pressure distribution under the metatarsal heads during walking. Arch support The role of intrinsic muscles in the support of the med- ial longitudinal arch has been investigated in both stand- ing [3-5] and walking [4,9]. Early EMG studies revealed that intrinsic foot muscles are not active during standing [3-5] and the plantar aponeurosis was widely accepted to Table 4 Database search strategy for SCOPUS Number Search terms Results* 1. foot 161105 2. muscle 1157744 3. intrinsic 239220 4. Number 1+2+3 349 5. Measure 1433899 6. Strength 891550 7. Number 1+2+3+5 21 8. Number 1+2+3+6 44 *The results are from the search conducted on the electronic database SCOPUS between May and June 2012. Table 5 Database search strategy for Cochrane Library Number Search terms Results* 1. foot 4650 2. muscle 23527 3. intrinsic 1436 4. Number 1+2+3 3 *The results are from the search conducted on the electronic database Cochrane Library between May and June 2012. Soysaet al. Journal of Foot and Ankle Research2012,5:29 Page 3 of 14 http://www.jfootankleres.com/content/5/1/29

be the primary structure responsible for arch support during rest [3,28,35,38]. However, a recent EMG study revealed a small amount of activity inabductor hallucis, flexor digitorum brevisand thequadratus plantaemus- cles during relaxed standing with a significant increase in activity with increased postural demands [41]. Reeser et al.[35] suggested that intrinsic foot muscles act as trusses for the longitudinal arches, to actively resist bending stresses during walking. This hypothesis is sup- ported by the findings that the plantar aponeurosis ten- sion drops significantly during late stance, while the arch height is increasing [42]. The lack of tension during late stance suggests that other structures such as intrinsic foot muscles may contribute to arch support during pro- pulsion. Furthermore a virtual study of the foot using the Finite Element Method has shown that mechanical stresses on the medial and lateral arch can be adjusted by plantar intrinsic muscles [43]. Therefore there is evi- dence that intrinsic muscles play an important role in the support of the medial longitudinal arch during gait and a small role in relaxed standing. Implications of intrinsic foot muscle weakness The next section will review the influence of intrinsic muscle weakness in the development of pes cavus in Charcot-Marie-Tooth disease, lesser toe deformities, hal- lux valgus and heel pain. Charcot-Marie-Tooth disease Charcot-Marie-Tooth disease (CMT) is a peripheral neuropathy, where anatomically distal muscles including the intrinsic muscles are preferentially affected [7]. Weakness of intrinsic foot muscles is a widely accepted pathological finding of CMT and Magnetic Resonance Imaging (MRI) studies have indicated significant atrophy in intrinsic foot muscles [6,7]. Several authors have hypothesised that intrinsic muscle weakness is an im- portant contributor to the development of pes cavus de- formity[44] [44,45]. One theory suggests that intrinsic muscle atrophy causes dorsiflexion of the MTP joints, due to the unopposed pull of the long extensors of the toe [44]. Dorsiflexion at the MTP joints elevates the lon- gitudinal arch by the windlass effect [44]. The continued imbalance leads to contracture in the plantar fascia and intrinsic muscles, which then pulls the forefoot into plantar flexion, leading to a progressively rigid cavus

dorsiflexion of the MTP joints, due to the unopposed pull of the long extensors of the toe [44]. Dorsiflexion at the MTP joints elevates the lon- gitudinal arch by the windlass effect [44]. The continued imbalance leads to contracture in the plantar fascia and intrinsic muscles, which then pulls the forefoot into plantar flexion, leading to a progressively rigid cavus foot [44,45]. However, a clear causal relationship between in- trinsic muscle weakness and the development of pes cavus foot has not been established and other theories of aetiology exist, such as extrinsic invertor-to-evertor muscle imbalance [7]. Without accurate means of evalu- ating intrinsic muscle strength, the role of intrinsic muscle atrophy in the development of pes cavus deform- ity will remain unknown. Lesser toe deformities Muscle imbalances between the intrinsic and extrinsic foot muscles have been proposed as the possible cause for lesser toe deformity [10,11,46]. Claw toe deformity is characterised by extension at the MTP joint with flexion of the proximal and distal interphalangeal joints [10]. Hammer toe is characterised by an extended MTP joint, flexed proximal interphalangeal joint and normal or extended distal interphalangeal joint [10]. Claw and hammer toe deformities are common in patients with diabetic neuropathy [47]. In an unaffected foot, the strong extension forces at the MTP joint by theextensor digitorum longus and brevisare balanced by the flexors forces produced by long and short toe flexors [10]. However, intrinsic muscle atrophy results in an imbalance of the extensor forces at the MTP joint, leading to the development of toe deformity [10]. The findings of Kwonet al.[11] support this theory, where participants with hammer toe deformity had greater dis- parity in the ratio of toe extensor-to-toe flexor muscle strength compared to the unaffected participants. How- ever, other mechanisms for the development of toe deformity have also been suggested such as restrictive footwear [10,46], rupture of plantar aponeurosis and joint capsule [10]. These alternative theories are supported by the findings of Bus and colleagues [20] in participants with diabetic neuropathy, whereby no difference in the degree of muscle atrophy was found in patients with and without claw

other mechanisms for the development of toe deformity have also been suggested such as restrictive footwear [10,46], rupture of plantar aponeurosis and joint capsule [10]. These alternative theories are supported by the findings of Bus and colleagues [20] in participants with diabetic neuropathy, whereby no difference in the degree of muscle atrophy was found in patients with and without claw deformity. However, a pilot study by Ledouxet al. [48] reported that both intrinsic muscle atrophy and increased plantar aponeurosis thickness were present in participants with claw toe deformity. Therefore, multiple factors may contribute to foot and toe deformity. Future prospective studies, measuring intrinsic muscle strength and plantar aponeurosis thickness, may help clarify this relationship. Hallux valgus Hallux valgus, orbunion, describes a foot deformity char- acterised by lateral deviation of the great toe at the MTP joint away from the midline of the body [46]. One proposed cause of hallux valgus deformity is a strength imbalance of theabductor halluciscompared to the adductor hallucis transverseandadductor hallucis oblique [12,13]. When the abductor muscles are weak, it has been suggested that the adductor force becomes dominant, pulling the great toe laterally at the MTP joint [12]. This theory is supported by muscle biopsy findings which revealed histological abnormalities and muscle fibre atro- phy in theabductor hallucismuscle in patients with symptomatic hallux valgus deformity [13]. Further studies, assessing muscle strength of the individual intrinsic mus- cles, are needed to better understand the pathogenesis of hallux valgus. Soysaet al. Journal of Foot and Ankle Research2012,5:29 Page 4 of 14 http://www.jfootankleres.com/content/5/1/29

Heel pain The role of the intrinsic muscle weakness in the devel- opment of plantar heel pain, or plantar fasciitis, is un- clear. One theory proposed by Allen and Gross [1] describes a relationship whereby weak intrinsic muscles provide insufficient dynamic truss support to the medial longitudinal arch, causing increased strain on the plantar aponeurosis. A MRI study by Changet al.[8] of partici- pants with chronic unilateral plantar fasciitis, reported a reduction of intrinsic muscle cross-sectional area in the forefoot of the symptomatic foot in comparison to the pain-free foot. The selected reduction of intrinsic foot muscle cross-sectional area in the forefoot and not the rearfoot is interesting because many intrinsic muscles have attachments into the first ray [8]. The atrophy of the intrinsic muscles may affect the stability of the med- ial longitudinal arch and therefore impede the healing process by further stressing the plantar aponeurosis [8]. Hence, intrinsic muscle weakness may play a significant role in chronic heel pain. However, further research, measuring intrinsic muscle strength prospectively, is needed to confirm this hypothesis. Measurement of intrinsic foot muscle strength The next section will review the‘direct’and‘indirect’ methods of measuring intrinsic muscle strength. The subheading‘direct methods of assessing intrinsic/extrin- sic muscle strength’reviews the methods that can dir- ectly measure a unit of force or power. However, these ‘direct’methods actually measure toe flexion strength which is a combination of intrinsic and extrinsic muscle strength. The subheading‘indirect methods of assessing intrinsic muscle strength’reviews methods that are un- able to directly measure force but provide information regarding intrinsic muscle structure and activity. Direct methods of assessing intrinsic/extrinsic muscle strength The direct methods reported in the literature include a variety of clinical tests [11,14,18,19,49,50] and laboratory based tests [15-17]. It is clear that the direct methods reported in the literature primarily measure toe flexor muscle force, while other actions such as toe extension and abduction force are rarely measured. Since toe flexor strength is a combination of intrinsic and extrinsic muscle activity all‘direct’methods are actually measur- ing intrinsic and extrinsic toe muscle strength. A variety of methods have been described that purport to measure

This review discusses the anatomy, implications of weakness, and measurement methods for intrinsic foot muscle strength.