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A cohort study of tibialis anterior tendon shortening in combination with calf muscle lengthening in spastic equinus in cerebral palsy
Gait & Posture 50 (2016) 23–27
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Full length article
A cohort study of tibialis anterior tendon shortening in combination with calf muscle lengthening in spastic equinus in cerebral palsy S.T.J. Tsanga,* , D. McMorranb , L. Robinsonb , J. Hermanc, J.E. Robbc, M.S. Gastona,c a
Department of Orthopaedics, Royal Hospital for Sick Children Edinburgh, 9 Sciennes Place, Edinburgh EH9 1LF, United Kingdom University of Edinburgh, College of Medicine and Veterinary Medicine, 49 Little France Crescent, Old Dalkeith Road, Edinburgh EH16 4SB, United Kingdom c The Anderson Gait Laboratory, SMART Centre, Astley Ainslie Hospital, 133 Grange Loan, Edinburgh EH9 2, United Kingdom b
A R T I C L E I N F O
Article history: Received 28 April 2016 Received in revised form 21 July 2016 Accepted 12 August 2016 Keywords: Cerebral palsy Equinus Gait
A B S T R A C T
The aim of this study was to evaluate the outcome of combined tibialis anterior tendon shortening (TATS) and calf muscle-tendon lengthening (CMTL) in spastic equinus. Prospectively collected data was analysed in 26 patients with hemiplegic (n = 13) and diplegic (n = 13) cerebral palsy (CP) (GMFCS level I or II, 14 males, 12 females, age range 10–35 years; mean 16.8 years). All patients had pre-operative 3D gait analysis and a further analysis at a mean of 17.1 months (5.6 months) after surgery. None was lost to follow-up. Twenty-eight combined TATS and CMTL were undertaken and 19 patients had additional synchronous multilevel surgery. At follow-up 79% of patients had improved foot positioning at initial contact, whilst 68% reported improved fitting or reduced requirement of orthotic support. Statistically significant improvements were seen in the Movement Analysis Profile for ankle dorsi-/plantarflexion (4.15 , p = 0.032), maximum ankle dorsiflexion during swing phase (11.68 , p < 0.001), and Edinburgh Visual Gait Score (EVGS) (4.85, p = 0.014). Diplegic patients had a greater improvement in the EVGS than hemiplegics (6.27 -vs- 2.21, p = 0.024). The originators of combined TATS and CMTL showed that it improved foot positioning during gait. The present study has independently confirmed favourable outcomes in a similar patient population and added additional outcome measures, the EVGS, foot positioning at initial contact, and maximum ankle dorsiflexion during swing phase. Study limitations include short term follow-up in a heterogeneous population and that 19 patients had additional surgery. TATS combined with CMTL is a recommended option for spastic equinus in ambulatory patients with CP. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction Equinus is the commonest deformity in cerebral palsy (CP) [1–3] and lengthening of a shortened gastrocnemius/soleus is commonly undertaken to improve gait. Previous studies have reported recurrent equinus after surgery in approximately 10–30% of patients with hemiplegia [4,5] and overcorrection resulting in a calcaneus heel in 3–30% of patients with spastic diplegia [6–8]. Although central weakness has been suggested by Lin et al. [9], the imbalance of agonist and antagonist muscle lengths across the ankle can also lead to additional functional weakness. In long standing equinus it is thought that the antagonist (tibialis anterior muscle-tendon unit) is elongated and therefore weakened, with the agonist (gastrocnemius/soleus muscle-tendon unit) shortened
* Corresponding author. E-mail address: [email protected] (S.T.J. Tsang). http://dx.doi.org/10.1016/j.gaitpost.2016.08.015 0966-6362/ã 2016 Elsevier B.V. All rights reserved.
and also weakened [10–12]. Although the range of dorsiflexion increases as a consequence of calf muscle-tendon lengthening (CMTL), additional therapy is often required to correct gait. It has been proposed that simultaneous tendon shortening of the antagonistic tibialis anterior tendon-muscle unit would help to rebalance muscle strength. Combined shortening of the anterior tibialis tendon-muscle unit and lengthening of the calf tendonmuscle unit in spastic equinus in CP has previously been described by Rutz et al. [13] and has been shown to improve foot positioning during gait. The Movement Analysis Profile (MAP) [14] has been developed to summarise kinematic data from three-dimensional (3D) instrumented gait analysis. The MAP describes the magnitude of deviation of nine individual variables averaged over the gait cycle. The Gait Profile Score (GPS) [14] reduces the MAP data to a single number that quantifies how much a gait pattern deviates from normal. The GPS is a single index outcome measure that summarises the overall quality of a patient’s gait kinematics and
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has been validated for evaluating outcomes [14]. The Edinburgh Visual Gait Score (EVGS) [15] consists of 17 items and is based on the visual observation of gait in the sagittal and coronal planes. It has been validated for use by experienced and inexperienced observers [16], has good concurrent validity with other assessments [17] and is reliable [18]. It has been shown to correlate strongly with the GPS and Gross Motor Function Classification System (GMFCS) [19]. The aim of this study was to evaluate the short-term outcome and the surgical results after tibialis anterior tendon shortening (TATS) in combination with calf muscle-tendon lengthening (CMTL) in spastic equinus in children with CP using the MAP, GPS, EVGS, foot position at initial contact, maximum ankle dorsiflexion during swing and orthoses use or fit. Our hypothesis was that this procedure would improve foot positioning during gait. 2. Methods and materials A retrospective analysis of prospectively collected data of all ambulatory children with CP and spastic equinus undergoing TATS in combination with CMTL was performed. All were performed at a single centre by the same surgeon between August 2011 and September 2014. Exclusion criteria were a diagnosis other than spastic cerebral palsy, dystonia or mixed movement disorder, Botulinum toxin A injections in the previous six months, gait improvement surgery within the preceding 18 months or GMFCS level III–V. All patients had pre- and post-operative 3D instrumented gait analysis undertaken in a **** accredited laboratory. The clinical assessment included the examination of the passive range of motion, spasticity according to the modified Ashworth/Bohannon scale [20] (scale: 0–4), the manual muscle strength test [21,22] (MRC scale: 0–5) of the ankle dorsi- and plantarflexors, a visual assessment of gait using the EVGS, and the use plus, if appropriate, fit of orthoses. The pre- and post-operative instrumented gait analysis included kinematics and kinetics, using a motion capture system (six camera VICON 460 system, Oxford Metrics Ltd., UK). Patients walked barefoot at a self-selected speed. The Helen Hayes Marker set [23] was used and at least three trials were recorded. Anthropometric data were recorded for appropriate scaling. All data were expressed as a percentage of the gait cycle using Polygon software (Oxford Metrics Ltd., UK). The MAP [14], GPS [14] and EVGS [15–17,24] were calculated for all patients pre- and postoperatively.
2.1. Surgical technique Posterior calf muscle lengthening was performed by recessing the proximal gastrocnemius and, if required, soleus aponeuroses. Following this the tibialis anterior tendon was exposed distal to the extensor retinaculum and freed of paratenon (Fig. 1). The ankle was placed into no more than 10 of dorsiflexion. The redundant tendon was then rolled around a pair of Gillies forceps to maximum tension and in such a way that the rolled-up excess tendon lay deep in the wound. The tension in the shortened tibialis anterior tendon was maintained by the assistant whilst a grasping whip stitch (using a pre-tensioned No. 6 Vicryl suture (Ethicon Inc., Johnson and Johnson)) was placed into the tendon. The suture was then anchored to the underlying navicular and medial cuneiform bones at the original insertion of tibialis anterior (Fig. 2). Post-operatively the foot was placed at a plantigrade position and held in a below knee cast which was split immediately. After two weeks the cast was changed to a plantigrade weight-bearing cast and retained for a further four weeks.
Fig. 1. Exposed tibialis tendon tensioned using Gillies forceps and a whip stitch (No. 6 Vicryl, Ethicon Inc., Johnson and Johnson). Cadaveric limb by courtesy of Professor *****, Professor of Translational anatomy, University of ****.
Fig. 2. Transosseous fixation of shortened tibialis anterior tendon to the medial cuneiform and navicular bones.
2.2. Statistics Testing for normality of the data was performed using the Shapiro-Wilk test. Paired data were assessed using the paired t-test or Wilcoxon’s matched-pairs signed ranks test or Chi-squared testing, where appropriate, and sequential data were assessed using repeated analysis of variance (ANOVA) with Bonferroni post hoc analysis (SPSS statistical software version 21.0, SPSS Inc., Chicago, Illinois). A p-value of <0.05 was considered to be statistically significant. 3. Results Twenty-six patients had 28 surgical interventions. Group I consisted of 13 patients with hemiplegic CP and group II of 13 patients with diplegic CP. The mean age of the patients was 16.8 years (sd 5.9 years, range 10.3–34.5 years) at the time of surgery. Four patients had undergone previous gait improvement surgery over 18 months prior to the combined TATS and CMTL surgery, and none had previous CMTL surgery. Nine patients were skeletally immature at the time of surgery. Additional, synchronous multilevel surgery was performed in 19 patients. Within the cohort 18 patients were GMFCS level I and eight were GMFCS level II. There were no statistical differences in patient demographics between the hemiplegic and diplegic patients (p < 0.05). There was a combined gastro-soleus contracture in eight limbs and an
S.T.J. Tsang et al. / Gait & Posture 50 (2016) 23–27
ipsilateral knee contracture in 19 limbs; soleal shortening was manged by soleus aponeurotomy and a knee contracture by semitendinosus tenotomy with or without a patella tendon shortening or distal femoral extension osteotomy. Poor selective control at the ankle was present in 11 limbs pre-operatively. Follow-up was performed at a mean 17.1 months (sd 5.6 months). Tables 1 and 2 show the kinematic results derived from instrumented and clinical gait analysis. Both groups showed improvement in the EVGS and maximum ankle dorsiflexion during swing. The overall improvement for mean EVGS was 4.85 (p = 0.014) and maximum ankle dorsiflexion was 11.68 (p < 0.001). Diplegic patients statistically had a greater improvement in the EVGS than hemiplegics (6.27 -vs- 2.21, p = 0.024). There was no statistical difference in the improvement seen for ankle dorsiflexion during swing between hemiplegic and diplegic patients (10.67 -vrs- 12.62 , p = 0.709). Only the hemiplegic group showed a statistically significant improvement for mean MAP ankle dorsiflexion with a change of 4.15 (p = 0.032). The mean MAP ankle dorsiflexion for the diplegic cohort showed an improvement of 4.33 but this was not statistically significant (p = 0.149). The MAP for pelvic rotation also improved in the diplegic cohort with a change of 2.98 (p = 0.028). None of the patients had an overcorrection of equinus at follow-up. Overall 22/28 (79%) of limbs showed an improvement in initial contact following surgery (Fig. 3). At follow-up fourteen limbs (50%) had improved ease of fitting into their ankle-foot orthoses (AFO), five limbs (18%) no longer required an AFO, and there was no change in seven limbs (25%) with ease of AFO fitting or requirement. Two limbs (7%) did not require AFO support preor post-operatively. All six limbs with no improved in foot positioning were found to have poor selective control preoperatively, this was found to be statistically significant (p = 0.001). There was no statistical difference in improvement of initial contact between hemiplegics and diplegics (p = 0.712). There was a mean improvement in peak A2 push-off power following the combined procedure (1.48 W -vs- 1.85 W) which approached statistical significance (p = 0.056). Across all outcome measures no statistically significant differences were found according to GMFCS level, skeletal maturity, or the presence of an ipsilateral knee contracture. There was one case of postoperative sural nerve neuropraxia which had resolved by the time of the follow up gait analysis.
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4. Discussion The originators of the combined TATS and CMTL showed that it improved foot positioning during gait [13]. The present study has independently confirmed favourable outcomes in a similar patient population in a different centre and added additional outcome measures; the EVGS, foot positioning at initial contact, maximum ankle dorsiflexion during swing phase, and effect on AFO use and fit. No patient had an overcorrection of equinus and there was an overall improvement in post-operative ankle MAP scores. Rutz et al. [13] hypothesised that with muscle contractures in CP the agonist is short whereas the antagonist becomes elongated, and that this overall contributes to muscle weakness. The active force generated by a muscle unit is maximal when the actin-myosin filament overlap is optimized and is proportionally decreased when overlap is diminished e.g. stretching or contracting beyond its optimal working length [25]. It is for this reason that the originators proposed agonist lengthening (CMTL) combined with antagonist shortening (TATS) at the ankle level. There is, however, debate in the literature as to the cause and the effect with regards to muscle weakness and changes in muscle unit length in CP. It has been postulated that primary antagonist muscle weakness rather than agonist spasticity may have a greater role in the development of deformity and functional disability in CP [10,26]. The CMTL/TATS procedure is analogous to the already established practice of hamstring lengthening and patella tendon shortening for knee flexion contractures and patellar tendon elongation [27,28]. The originators of the procedure [13] found that diplegic patients had greater improvements in mean MAP ankle dorsiflexion, MAP foot progression, GPS, Gait Deviation Index and Gillette Gait Index to the combined procedure than hemiplegic patients. Similar outcomes were seen in the present study as diplegic patients showed a statistically greater improvement than the hemiplegic group in the EVGS (6.27 -vs- 2.21, p = 0.024). The MAP ankle dorsiflexion also improved in both groups but was only statistically significant in hemiplegics (p = 0.032). Ferriera et al. [29] found a 48% mean improvement in MAP ankle dorsiflexion 12 months following percutaneous gastrocnemius lengthening (Vulpius technique) in a mixed cohort of 19 skeletally-immature children with CP. There was a similar mean improvement (Pre-op 11.09 vs Post-op 6.94 , 37%) seen amongst the hemiplegic patients in the present study. However the patients evaluated by Ferreira et al. had a greater mean pre-operative deviation from a normal
Table 1 Kinematic results (Mean standard deviation) derived from instrumented 3D and clinical gait analysis for hemiplegic cohort. Statistically significant changes are shown in bold. Group I (n = 13, 13 operated lower limbs) Pre-operative
Post-operative
p-value
MAP pelvic tilt MAP pelvic obliquity MAP pelvic rotation MAP hip flexion/extension MAP hip add/abduction MAP hip rotation MAP knee flexion/extension MAP ankle dorsi/plantarflexion MAP foot progression
7.46 7.67 3.52 2.50 5.27 3.36 12.94 7.20 5.04 2.30 10.00 7.69 13.81 5.75 11.09 3.92 15.00 7.85
7.53 7.29 3.77 2.83 5.03 1.88 11.43 7.29 4.34 2.38 11.66 7.84 11.89 6.00 6.94 2.24 10.89 5.41
0.317 0.461 0.086 0.107 0.544 1.000 0.205 0.032a 0.130
GPS
9.50 2.71
9.09 2.73
0.333
EVGS operated limb EVGS non-operated limb EVGS total
10.21 3.07 9.71 3.86 13.00 5.87
8.29 3.91 2.50 2.94 10.79 6.55
<0.01a <0.001a 0.014a
Maximum ankle dorsiflexion during swing phasea ( )
3.41 12.83
14.08 4.60
<0.01a
a
Derived from instrumented 3D gait analysis.
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S.T.J. Tsang et al. / Gait & Posture 50 (2016) 23–27
Table 2 Kinematic results (Mean standard deviation) derived from instrumented 3D and clinical gait analysis for diplegic cohort. Statistically significant changes are shown in bold. Group II (n = 13, 15 operated lower limbs) Pre-operative
Post-operative
p-value
MAP pelvic tilt MAP pelvic obliquity MAP pelvic rotation MAP hip flexion/extension MAP hip add/abduction MAP hip rotation MAP knee flexion/extension MAP ankle dorsi/plantarflexion MAP foot progression
13.30 7.20 3.95 1.95 8.59 5.96 20.74 9.00 6.10 3.84 12.59 7.95 17.90 7.72 13.11 14.00 13.66 7.85
14.87 7.82 4.84 5.11 5.61 4.21 19.88 7.60 5.98 4.62 10.94 6.91 15.40 10.51 8.78 3.96 10.89 5.41
0.317 0.461 0.028a 0.107 0.544 1.000 0.205 0.149 0.130
GPS
13.51 4.37
11.88 3.88
0.178
EVGS operated limb EVGS non-operated limb EVGS total
12.91 5.45 11.00 3.57 24.42 9.66
8.86 5.21 7.83 5.98 18.15 10.06
<0.01a <0.001a 0.014a
Maximum ankle dorsiflexion during swing phasea ( )
4.61 15.27
17.23 8.08
<0.001a
a
Derived from instrumented 3D gait analysis.
gait (Pre-op 22.2 vs Pre-op 11.09 ). There was also improvement in the MAP pelvic rotation in the diplegic cohort in the present study. This is most likely to have been due to synchronous bilateral femoral de-rotation osteotomies (proximal varus (1/6) and distal extension (5/6)) at the time of their equinus correction rather than the combined procedure itself. A greater mean improvement in the EVGS of the non-operated compared to the operated limb ( 7.21 vs 1.92) was seen in the hemiplegic group (Table 1). In all patients the operated limb was the affected limb. The high pre-operative scores may have been due to the indirect effects of the affected limb on the contralateral limb during gait, such as excessive pelvic tilt and trunk movement to gain adequate swing clearance. The unaffected limb demonstrated a greater return to “normal” than the affected limb. Rutz et al. [13] reported fewer patients (9/29) who had improved foot positioning in gait after surgery than in this study (22/28). Ounpuu et al. [30] examined the effect of single-event multi-level soft tissue corrections (rectus tendon transfer, hamstring and gastrocnemius lengthening) in a group of 22 skeletallyimmature patients, GMFCS I–III. At twelve months post-procedure mean ankle position during initial contact was flatfoot (0 ) with a mean dorsiflexion during swing of 6 , both of which were smaller
Fig. 3. Diagram demonstrating effect of combined calf muscle-tendon lengthening (CMTL) and tibialis anterior tendon shortening (TATS) on foot positioning at initial contact. Each point represents one foot.
improvements in comparison with our study. The patients in the present study who did not have improved foot prepositioning all had poor selective control of tibialis anterior pre-operatively. In those demonstrating control of tibialis anterior with triple flexion (n = 5) there was a single level of improvement of toe contact to foot flat contact. All patients who had two levels of improvement from toe contact to heel contact had adequate selective control of tibialis anterior pre-operatively (Fig. 3). We feel this is an important consideration when considering the CMTL/TATS procedure combined procedure and that patients who do not demonstrate active function in the tibialis anterior preoperatively, including during a triple flexion pattern during gait, should probably not undergo the TATS part of the procedure. These patients are highly likely to remain reliant on their AFO. On the other hand, patients who have reasonable control over tibialis anterior, even during the more primitive triple flexion, can be considered to discontinue their AFO use if they demonstrate good tibialis anterior function and heel positioning out of AFO at the medium term post-operative follow up. This is an important motivator in these patients, who often dislike the cosmetic and social effects of the AFO. Rutz et al. found that even in their patients who had improved foot positioning there was no demonstrable clinical improvement in the strength of the gastro-soleus and tibialis anterior muscles [13]. It is likely that underlying muscle patterning and neuromuscular control remains unchanged in spite of the functional improvements after this procedure. In the present study the effect on foot positioning from surgery was found to improve the fit of orthoses (14/28) and even reduce their requirement (5/28). The limitations of this study include lack of a control group, short term follow-up in a heterogeneous population and that 19 patients had additional surgery. However, distinguishing between the natural history of CP and interventions and isolating the effects of one intervention from others in multilevel surgery are well recognised difficulties in cohort studies in CP. This should be considered when interpreting the effects on global evaluations of gait such as GPS and EVGS. A study with mid- to long-term followup may clarify the latter effects of the combined procedure. Additionally the outcomes of the procedure in GMFCS III patients is unknown. The present study has independently confirmed favourable outcomes of combined TATS with CMTL. It has been found to be reproducible in terms of safety and efficacy. TATS combined with CMTL is a recommended option for spastic equinus in ambulatory
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patients with CP but patients should have active dorsiflexion preoperatively. Acknowledgements The authors would like to thank Professor Gordon Findlater, Professor of Translational Anatomy, University of Edinburgh and his department staff for providing the cadaveric limb used in the images within this article. Conflict of interest None. References [1] A.D. Grant, R. Feldman, W.B. Lehman, Equinus deformity in cerebral palsy: a retrospective analysis of treatment and function in 39 cases, J. Pediatr. Orthop. 5 (January (6)) (2016) 678–681. [2] H.K. Graham, J.A. Fixsen, Lengthening of the calcaneal tendon in spastic hemiplegia by the White slide technique. A long-term review, J. Bone Joint Surg. Br. 70 (May (3)) (1988) 472–475. [3] H. Kerr Graham, P. Selber, Musculoskeletal aspects of cerebral palsy, J. Bone Joint Surg. Br. 85 (March (2)) (2003) 157–166. [4] T.A. Damron, T.A. Greenwald, A.L. Breed, Chronologic outcome of surgical tendoachilles lengthening and natural history of gastroc-soleus contracture in cerebral palsy. A two-part study, Clin. Orthop. Relat. Res. 301 (April) (1994) 249–255. [5] D.C. Borton, K. Walker, M. Pirpiris, G.R. Nattrass, H.K. Graham, Isolated calf lengthening in cerebral palsy. Outcome analysis of risk factors, J. Bone Joint Surg. Br. 83 (April (3)) (2001) 364–370. [6] A.H. Pierrot, O.B. Murphy, Albert E. Klinkicht Award, 1972. Heel cord advancement. A new approach to the spastic equinus deformity, Orthop. Clin. North Am. 5 (1) (1974) 117–126. [7] G.E. Fulford, Surgical management of ankle and foot deformities in cerebral palsy, Clin. Orthop. Relat. Res. 253 (April) (1990) 55–61. [8] J.J. Craig, J. van Vuren, The importance of gastrocnemius recession in the correction of equinus deformity in cerebral palsy, J. Bone Joint Surg. Br. 58 (March (1)) (1976) 84–87. [9] J.P. Lin, J.K. Brown, Peripheral and central mechanisms of hindfoot equinus in childhood hemiplegia, Dev. Med. Child Neurol. 34 (November (11)) (1992) 949–965. [10] D.C. Bland, L.A. Prosser, L.A. Bellini, K.E. Alter, D.L. Damiano, Tibialis anterior architecture, strength, and gait in individuals with cerebral palsy, Muscle Nerve 44 (4) (2011) 509–517. [11] R. Brunner, Muscle physiology and the effect of muscle-tendon surgery in cerebral palsy, Der Orthopäde 33 (October (10)) (2004) 1096–1102. [12] M. Mockford, J.M. Caulton, The pathophysiological basis of weakness in children with cerebral palsy, Paediatr. Phys. Ther. 22 (2) (2010) 222–233.
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[13] E. Rutz, R. Baker, O. Tirosh, J. Romkes, C. Haase, R. Brunner, Tibialis anterior tendon shortening in combination with Achilles tendon lengthening in spastic equinus in cerebral palsy, Gait Posture 33 (February (2)) (2011) 152–157. [14] R. Baker, J.L. McGinley, M.H. Schwartz, S. Beynon, A. Rozumalski, H.K. Graham, et al., The gait profile score and movement analysis profile, Gait Posture 30 (October (3)) (2009) 265–269. [15] H.S. Read, M.E. Hazlewood, S.J. Hillman, R.J. Prescott, J.E. Robb, Edinburgh visual gait score for use in cerebral palsy, J. Pediatr. Orthop. 23 (January (3)) (2016) 296–301. [16] A.M.L. Ong, S.J. Hillman, J.E. Robb, Reliability and validity of the Edinburgh Visual Gait Score for cerebral palsy when used by inexperienced observers, Gait Posture 28 (August (2)) (2008) 323–326. [17] S.J. Hillman, M.E. Hazlewood, M.H. Schwartz, M.L. van der Linden, J.E. Robb, Correlation of the Edinburgh Gait Score with the Gillette Gait Index, the Gillette Functional Assessment Questionnaire, and dimensionless speed, J. Pediatr. Orthop. 27 (January (1)) (2016) 7–11. [18] C. Rathinam, A. Bateman, J. Peirson, J. Skinner, Observational gait assessment tools in paediatrics—a systematic review, Gait Posture 40 (June (2)) (2014) 279–285. [19] L.W. Robinson, N. Clement, M. Fullarton, A. Richardson, J. Herman, G. Henderson, et al., The relationship between the Edinburgh Visual Gait Score, the Gait Profile Score and GMFCS levels I-III, Gait Posture 41 (February (2)) (2015) 741–743. [20] R.W. Bohannon, M.B. Smith, Interrater reliability of a modified Ashworth scale of muscle spasticity, Phys. Ther. 67 (February (2)) (1987) 206–207. [21] J.R. Mendell, J. Florence, Manual muscle testing, Muscle Nerve 13 (January (Suppl. S16–20)) (1990). [22] S.C. Cuthbert, G.J. Goodheart, On the reliability and validity of manual muscle testing: a literature review, Chiropr. Osteopat. 15 (January) (2007) 4.A. [23] M.P. Kadaba, H.K. Ramakrishnan, M.E. Wootten, Measurement of lower extremity kinematics during level walking, J. Orthop. Res. 8 (May (3)) (1990) 383–392. [24] S. Gupta, K. Raja, Responsiveness of Edinburgh Visual Gait Score to orthopedic surgical intervention of the lower limbs in children with cerebral palsy, Am. J. Phys. Med. Rehabil. 91 (October (9)) (2012) 761–767. [25] D.E. Rassier, B.R. MacIntosh, W. Herzog, Length dependence of active force production in skeletal muscle, J. Appl. Physiol. 86 (May 1 (5)) (1999) 1445–1457. [26] S. Levitt, The Pathophysiological Basis of Weakness in Children With Cerebral Palsy, 5th ed., Wiley-Blackwell, Oxford: Malden, Mass, 2010 356 p.. [27] D.B. Lotman, Knee flexion deformity and patella alta in spastic cerebral palsy, Dev. Med. Child Neurol. 18 (June (3)) (1976) 315–319. [28] R.K. Beals, Treatment of knee contracture in cerebral palsy by hamstring lengthening, posterior capsulotomy, and quadriceps mechanism shortening, Dev. Med. Child Neurol. 43 (February 13 (12)) (2007) 802–805. [29] L.A.B. Ferreira, V. Cimolin, P.F. Costici, G. Albertini, C.S. Oliveira, M. Galli, Effects of gastrocnemius fascia lengthening on gait pattern in children with cerebral palsy using the gait profile score, Res. Dev. Disabil. 35 (2014) 1137–1143. [30] S. Ounpuu, M. Solomito, K. Bell, P. DeLuca, K. Pierz, Long-term outcomes after multilevel surgery including rectus femoris, hamstring and gastrocnemius procedures in children with cerebral palsy, Gait Posture 42 (2015) 365–372.
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Full length article
A cohort study of tibialis anterior tendon shortening in combination with calf muscle lengthening in spastic equinus in cerebral palsy S.T.J. Tsanga,* , D. McMorranb , L. Robinsonb , J. Hermanc, J.E. Robbc, M.S. Gastona,c a
Department of Orthopaedics, Royal Hospital for Sick Children Edinburgh, 9 Sciennes Place, Edinburgh EH9 1LF, United Kingdom University of Edinburgh, College of Medicine and Veterinary Medicine, 49 Little France Crescent, Old Dalkeith Road, Edinburgh EH16 4SB, United Kingdom c The Anderson Gait Laboratory, SMART Centre, Astley Ainslie Hospital, 133 Grange Loan, Edinburgh EH9 2, United Kingdom b
A R T I C L E I N F O
Article history: Received 28 April 2016 Received in revised form 21 July 2016 Accepted 12 August 2016 Keywords: Cerebral palsy Equinus Gait
A B S T R A C T
The aim of this study was to evaluate the outcome of combined tibialis anterior tendon shortening (TATS) and calf muscle-tendon lengthening (CMTL) in spastic equinus. Prospectively collected data was analysed in 26 patients with hemiplegic (n = 13) and diplegic (n = 13) cerebral palsy (CP) (GMFCS level I or II, 14 males, 12 females, age range 10–35 years; mean 16.8 years). All patients had pre-operative 3D gait analysis and a further analysis at a mean of 17.1 months (5.6 months) after surgery. None was lost to follow-up. Twenty-eight combined TATS and CMTL were undertaken and 19 patients had additional synchronous multilevel surgery. At follow-up 79% of patients had improved foot positioning at initial contact, whilst 68% reported improved fitting or reduced requirement of orthotic support. Statistically significant improvements were seen in the Movement Analysis Profile for ankle dorsi-/plantarflexion (4.15 , p = 0.032), maximum ankle dorsiflexion during swing phase (11.68 , p < 0.001), and Edinburgh Visual Gait Score (EVGS) (4.85, p = 0.014). Diplegic patients had a greater improvement in the EVGS than hemiplegics (6.27 -vs- 2.21, p = 0.024). The originators of combined TATS and CMTL showed that it improved foot positioning during gait. The present study has independently confirmed favourable outcomes in a similar patient population and added additional outcome measures, the EVGS, foot positioning at initial contact, and maximum ankle dorsiflexion during swing phase. Study limitations include short term follow-up in a heterogeneous population and that 19 patients had additional surgery. TATS combined with CMTL is a recommended option for spastic equinus in ambulatory patients with CP. ã 2016 Elsevier B.V. All rights reserved.
1. Introduction Equinus is the commonest deformity in cerebral palsy (CP) [1–3] and lengthening of a shortened gastrocnemius/soleus is commonly undertaken to improve gait. Previous studies have reported recurrent equinus after surgery in approximately 10–30% of patients with hemiplegia [4,5] and overcorrection resulting in a calcaneus heel in 3–30% of patients with spastic diplegia [6–8]. Although central weakness has been suggested by Lin et al. [9], the imbalance of agonist and antagonist muscle lengths across the ankle can also lead to additional functional weakness. In long standing equinus it is thought that the antagonist (tibialis anterior muscle-tendon unit) is elongated and therefore weakened, with the agonist (gastrocnemius/soleus muscle-tendon unit) shortened
* Corresponding author. E-mail address: [email protected] (S.T.J. Tsang). http://dx.doi.org/10.1016/j.gaitpost.2016.08.015 0966-6362/ã 2016 Elsevier B.V. All rights reserved.
and also weakened [10–12]. Although the range of dorsiflexion increases as a consequence of calf muscle-tendon lengthening (CMTL), additional therapy is often required to correct gait. It has been proposed that simultaneous tendon shortening of the antagonistic tibialis anterior tendon-muscle unit would help to rebalance muscle strength. Combined shortening of the anterior tibialis tendon-muscle unit and lengthening of the calf tendonmuscle unit in spastic equinus in CP has previously been described by Rutz et al. [13] and has been shown to improve foot positioning during gait. The Movement Analysis Profile (MAP) [14] has been developed to summarise kinematic data from three-dimensional (3D) instrumented gait analysis. The MAP describes the magnitude of deviation of nine individual variables averaged over the gait cycle. The Gait Profile Score (GPS) [14] reduces the MAP data to a single number that quantifies how much a gait pattern deviates from normal. The GPS is a single index outcome measure that summarises the overall quality of a patient’s gait kinematics and
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has been validated for evaluating outcomes [14]. The Edinburgh Visual Gait Score (EVGS) [15] consists of 17 items and is based on the visual observation of gait in the sagittal and coronal planes. It has been validated for use by experienced and inexperienced observers [16], has good concurrent validity with other assessments [17] and is reliable [18]. It has been shown to correlate strongly with the GPS and Gross Motor Function Classification System (GMFCS) [19]. The aim of this study was to evaluate the short-term outcome and the surgical results after tibialis anterior tendon shortening (TATS) in combination with calf muscle-tendon lengthening (CMTL) in spastic equinus in children with CP using the MAP, GPS, EVGS, foot position at initial contact, maximum ankle dorsiflexion during swing and orthoses use or fit. Our hypothesis was that this procedure would improve foot positioning during gait. 2. Methods and materials A retrospective analysis of prospectively collected data of all ambulatory children with CP and spastic equinus undergoing TATS in combination with CMTL was performed. All were performed at a single centre by the same surgeon between August 2011 and September 2014. Exclusion criteria were a diagnosis other than spastic cerebral palsy, dystonia or mixed movement disorder, Botulinum toxin A injections in the previous six months, gait improvement surgery within the preceding 18 months or GMFCS level III–V. All patients had pre- and post-operative 3D instrumented gait analysis undertaken in a **** accredited laboratory. The clinical assessment included the examination of the passive range of motion, spasticity according to the modified Ashworth/Bohannon scale [20] (scale: 0–4), the manual muscle strength test [21,22] (MRC scale: 0–5) of the ankle dorsi- and plantarflexors, a visual assessment of gait using the EVGS, and the use plus, if appropriate, fit of orthoses. The pre- and post-operative instrumented gait analysis included kinematics and kinetics, using a motion capture system (six camera VICON 460 system, Oxford Metrics Ltd., UK). Patients walked barefoot at a self-selected speed. The Helen Hayes Marker set [23] was used and at least three trials were recorded. Anthropometric data were recorded for appropriate scaling. All data were expressed as a percentage of the gait cycle using Polygon software (Oxford Metrics Ltd., UK). The MAP [14], GPS [14] and EVGS [15–17,24] were calculated for all patients pre- and postoperatively.
2.1. Surgical technique Posterior calf muscle lengthening was performed by recessing the proximal gastrocnemius and, if required, soleus aponeuroses. Following this the tibialis anterior tendon was exposed distal to the extensor retinaculum and freed of paratenon (Fig. 1). The ankle was placed into no more than 10 of dorsiflexion. The redundant tendon was then rolled around a pair of Gillies forceps to maximum tension and in such a way that the rolled-up excess tendon lay deep in the wound. The tension in the shortened tibialis anterior tendon was maintained by the assistant whilst a grasping whip stitch (using a pre-tensioned No. 6 Vicryl suture (Ethicon Inc., Johnson and Johnson)) was placed into the tendon. The suture was then anchored to the underlying navicular and medial cuneiform bones at the original insertion of tibialis anterior (Fig. 2). Post-operatively the foot was placed at a plantigrade position and held in a below knee cast which was split immediately. After two weeks the cast was changed to a plantigrade weight-bearing cast and retained for a further four weeks.
Fig. 1. Exposed tibialis tendon tensioned using Gillies forceps and a whip stitch (No. 6 Vicryl, Ethicon Inc., Johnson and Johnson). Cadaveric limb by courtesy of Professor *****, Professor of Translational anatomy, University of ****.
Fig. 2. Transosseous fixation of shortened tibialis anterior tendon to the medial cuneiform and navicular bones.
2.2. Statistics Testing for normality of the data was performed using the Shapiro-Wilk test. Paired data were assessed using the paired t-test or Wilcoxon’s matched-pairs signed ranks test or Chi-squared testing, where appropriate, and sequential data were assessed using repeated analysis of variance (ANOVA) with Bonferroni post hoc analysis (SPSS statistical software version 21.0, SPSS Inc., Chicago, Illinois). A p-value of <0.05 was considered to be statistically significant. 3. Results Twenty-six patients had 28 surgical interventions. Group I consisted of 13 patients with hemiplegic CP and group II of 13 patients with diplegic CP. The mean age of the patients was 16.8 years (sd 5.9 years, range 10.3–34.5 years) at the time of surgery. Four patients had undergone previous gait improvement surgery over 18 months prior to the combined TATS and CMTL surgery, and none had previous CMTL surgery. Nine patients were skeletally immature at the time of surgery. Additional, synchronous multilevel surgery was performed in 19 patients. Within the cohort 18 patients were GMFCS level I and eight were GMFCS level II. There were no statistical differences in patient demographics between the hemiplegic and diplegic patients (p < 0.05). There was a combined gastro-soleus contracture in eight limbs and an
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ipsilateral knee contracture in 19 limbs; soleal shortening was manged by soleus aponeurotomy and a knee contracture by semitendinosus tenotomy with or without a patella tendon shortening or distal femoral extension osteotomy. Poor selective control at the ankle was present in 11 limbs pre-operatively. Follow-up was performed at a mean 17.1 months (sd 5.6 months). Tables 1 and 2 show the kinematic results derived from instrumented and clinical gait analysis. Both groups showed improvement in the EVGS and maximum ankle dorsiflexion during swing. The overall improvement for mean EVGS was 4.85 (p = 0.014) and maximum ankle dorsiflexion was 11.68 (p < 0.001). Diplegic patients statistically had a greater improvement in the EVGS than hemiplegics (6.27 -vs- 2.21, p = 0.024). There was no statistical difference in the improvement seen for ankle dorsiflexion during swing between hemiplegic and diplegic patients (10.67 -vrs- 12.62 , p = 0.709). Only the hemiplegic group showed a statistically significant improvement for mean MAP ankle dorsiflexion with a change of 4.15 (p = 0.032). The mean MAP ankle dorsiflexion for the diplegic cohort showed an improvement of 4.33 but this was not statistically significant (p = 0.149). The MAP for pelvic rotation also improved in the diplegic cohort with a change of 2.98 (p = 0.028). None of the patients had an overcorrection of equinus at follow-up. Overall 22/28 (79%) of limbs showed an improvement in initial contact following surgery (Fig. 3). At follow-up fourteen limbs (50%) had improved ease of fitting into their ankle-foot orthoses (AFO), five limbs (18%) no longer required an AFO, and there was no change in seven limbs (25%) with ease of AFO fitting or requirement. Two limbs (7%) did not require AFO support preor post-operatively. All six limbs with no improved in foot positioning were found to have poor selective control preoperatively, this was found to be statistically significant (p = 0.001). There was no statistical difference in improvement of initial contact between hemiplegics and diplegics (p = 0.712). There was a mean improvement in peak A2 push-off power following the combined procedure (1.48 W -vs- 1.85 W) which approached statistical significance (p = 0.056). Across all outcome measures no statistically significant differences were found according to GMFCS level, skeletal maturity, or the presence of an ipsilateral knee contracture. There was one case of postoperative sural nerve neuropraxia which had resolved by the time of the follow up gait analysis.
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4. Discussion The originators of the combined TATS and CMTL showed that it improved foot positioning during gait [13]. The present study has independently confirmed favourable outcomes in a similar patient population in a different centre and added additional outcome measures; the EVGS, foot positioning at initial contact, maximum ankle dorsiflexion during swing phase, and effect on AFO use and fit. No patient had an overcorrection of equinus and there was an overall improvement in post-operative ankle MAP scores. Rutz et al. [13] hypothesised that with muscle contractures in CP the agonist is short whereas the antagonist becomes elongated, and that this overall contributes to muscle weakness. The active force generated by a muscle unit is maximal when the actin-myosin filament overlap is optimized and is proportionally decreased when overlap is diminished e.g. stretching or contracting beyond its optimal working length [25]. It is for this reason that the originators proposed agonist lengthening (CMTL) combined with antagonist shortening (TATS) at the ankle level. There is, however, debate in the literature as to the cause and the effect with regards to muscle weakness and changes in muscle unit length in CP. It has been postulated that primary antagonist muscle weakness rather than agonist spasticity may have a greater role in the development of deformity and functional disability in CP [10,26]. The CMTL/TATS procedure is analogous to the already established practice of hamstring lengthening and patella tendon shortening for knee flexion contractures and patellar tendon elongation [27,28]. The originators of the procedure [13] found that diplegic patients had greater improvements in mean MAP ankle dorsiflexion, MAP foot progression, GPS, Gait Deviation Index and Gillette Gait Index to the combined procedure than hemiplegic patients. Similar outcomes were seen in the present study as diplegic patients showed a statistically greater improvement than the hemiplegic group in the EVGS (6.27 -vs- 2.21, p = 0.024). The MAP ankle dorsiflexion also improved in both groups but was only statistically significant in hemiplegics (p = 0.032). Ferriera et al. [29] found a 48% mean improvement in MAP ankle dorsiflexion 12 months following percutaneous gastrocnemius lengthening (Vulpius technique) in a mixed cohort of 19 skeletally-immature children with CP. There was a similar mean improvement (Pre-op 11.09 vs Post-op 6.94 , 37%) seen amongst the hemiplegic patients in the present study. However the patients evaluated by Ferreira et al. had a greater mean pre-operative deviation from a normal
Table 1 Kinematic results (Mean standard deviation) derived from instrumented 3D and clinical gait analysis for hemiplegic cohort. Statistically significant changes are shown in bold. Group I (n = 13, 13 operated lower limbs) Pre-operative
Post-operative
p-value
MAP pelvic tilt MAP pelvic obliquity MAP pelvic rotation MAP hip flexion/extension MAP hip add/abduction MAP hip rotation MAP knee flexion/extension MAP ankle dorsi/plantarflexion MAP foot progression
7.46 7.67 3.52 2.50 5.27 3.36 12.94 7.20 5.04 2.30 10.00 7.69 13.81 5.75 11.09 3.92 15.00 7.85
7.53 7.29 3.77 2.83 5.03 1.88 11.43 7.29 4.34 2.38 11.66 7.84 11.89 6.00 6.94 2.24 10.89 5.41
0.317 0.461 0.086 0.107 0.544 1.000 0.205 0.032a 0.130
GPS
9.50 2.71
9.09 2.73
0.333
EVGS operated limb EVGS non-operated limb EVGS total
10.21 3.07 9.71 3.86 13.00 5.87
8.29 3.91 2.50 2.94 10.79 6.55
<0.01a <0.001a 0.014a
Maximum ankle dorsiflexion during swing phasea ( )
3.41 12.83
14.08 4.60
<0.01a
a
Derived from instrumented 3D gait analysis.
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Table 2 Kinematic results (Mean standard deviation) derived from instrumented 3D and clinical gait analysis for diplegic cohort. Statistically significant changes are shown in bold. Group II (n = 13, 15 operated lower limbs) Pre-operative
Post-operative
p-value
MAP pelvic tilt MAP pelvic obliquity MAP pelvic rotation MAP hip flexion/extension MAP hip add/abduction MAP hip rotation MAP knee flexion/extension MAP ankle dorsi/plantarflexion MAP foot progression
13.30 7.20 3.95 1.95 8.59 5.96 20.74 9.00 6.10 3.84 12.59 7.95 17.90 7.72 13.11 14.00 13.66 7.85
14.87 7.82 4.84 5.11 5.61 4.21 19.88 7.60 5.98 4.62 10.94 6.91 15.40 10.51 8.78 3.96 10.89 5.41
0.317 0.461 0.028a 0.107 0.544 1.000 0.205 0.149 0.130
GPS
13.51 4.37
11.88 3.88
0.178
EVGS operated limb EVGS non-operated limb EVGS total
12.91 5.45 11.00 3.57 24.42 9.66
8.86 5.21 7.83 5.98 18.15 10.06
<0.01a <0.001a 0.014a
Maximum ankle dorsiflexion during swing phasea ( )
4.61 15.27
17.23 8.08
<0.001a
a
Derived from instrumented 3D gait analysis.
gait (Pre-op 22.2 vs Pre-op 11.09 ). There was also improvement in the MAP pelvic rotation in the diplegic cohort in the present study. This is most likely to have been due to synchronous bilateral femoral de-rotation osteotomies (proximal varus (1/6) and distal extension (5/6)) at the time of their equinus correction rather than the combined procedure itself. A greater mean improvement in the EVGS of the non-operated compared to the operated limb ( 7.21 vs 1.92) was seen in the hemiplegic group (Table 1). In all patients the operated limb was the affected limb. The high pre-operative scores may have been due to the indirect effects of the affected limb on the contralateral limb during gait, such as excessive pelvic tilt and trunk movement to gain adequate swing clearance. The unaffected limb demonstrated a greater return to “normal” than the affected limb. Rutz et al. [13] reported fewer patients (9/29) who had improved foot positioning in gait after surgery than in this study (22/28). Ounpuu et al. [30] examined the effect of single-event multi-level soft tissue corrections (rectus tendon transfer, hamstring and gastrocnemius lengthening) in a group of 22 skeletallyimmature patients, GMFCS I–III. At twelve months post-procedure mean ankle position during initial contact was flatfoot (0 ) with a mean dorsiflexion during swing of 6 , both of which were smaller
Fig. 3. Diagram demonstrating effect of combined calf muscle-tendon lengthening (CMTL) and tibialis anterior tendon shortening (TATS) on foot positioning at initial contact. Each point represents one foot.
improvements in comparison with our study. The patients in the present study who did not have improved foot prepositioning all had poor selective control of tibialis anterior pre-operatively. In those demonstrating control of tibialis anterior with triple flexion (n = 5) there was a single level of improvement of toe contact to foot flat contact. All patients who had two levels of improvement from toe contact to heel contact had adequate selective control of tibialis anterior pre-operatively (Fig. 3). We feel this is an important consideration when considering the CMTL/TATS procedure combined procedure and that patients who do not demonstrate active function in the tibialis anterior preoperatively, including during a triple flexion pattern during gait, should probably not undergo the TATS part of the procedure. These patients are highly likely to remain reliant on their AFO. On the other hand, patients who have reasonable control over tibialis anterior, even during the more primitive triple flexion, can be considered to discontinue their AFO use if they demonstrate good tibialis anterior function and heel positioning out of AFO at the medium term post-operative follow up. This is an important motivator in these patients, who often dislike the cosmetic and social effects of the AFO. Rutz et al. found that even in their patients who had improved foot positioning there was no demonstrable clinical improvement in the strength of the gastro-soleus and tibialis anterior muscles [13]. It is likely that underlying muscle patterning and neuromuscular control remains unchanged in spite of the functional improvements after this procedure. In the present study the effect on foot positioning from surgery was found to improve the fit of orthoses (14/28) and even reduce their requirement (5/28). The limitations of this study include lack of a control group, short term follow-up in a heterogeneous population and that 19 patients had additional surgery. However, distinguishing between the natural history of CP and interventions and isolating the effects of one intervention from others in multilevel surgery are well recognised difficulties in cohort studies in CP. This should be considered when interpreting the effects on global evaluations of gait such as GPS and EVGS. A study with mid- to long-term followup may clarify the latter effects of the combined procedure. Additionally the outcomes of the procedure in GMFCS III patients is unknown. The present study has independently confirmed favourable outcomes of combined TATS with CMTL. It has been found to be reproducible in terms of safety and efficacy. TATS combined with CMTL is a recommended option for spastic equinus in ambulatory
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patients with CP but patients should have active dorsiflexion preoperatively. Acknowledgements The authors would like to thank Professor Gordon Findlater, Professor of Translational Anatomy, University of Edinburgh and his department staff for providing the cadaveric limb used in the images within this article. Conflict of interest None. References [1] A.D. Grant, R. Feldman, W.B. Lehman, Equinus deformity in cerebral palsy: a retrospective analysis of treatment and function in 39 cases, J. Pediatr. Orthop. 5 (January (6)) (2016) 678–681. [2] H.K. Graham, J.A. Fixsen, Lengthening of the calcaneal tendon in spastic hemiplegia by the White slide technique. A long-term review, J. Bone Joint Surg. Br. 70 (May (3)) (1988) 472–475. [3] H. Kerr Graham, P. Selber, Musculoskeletal aspects of cerebral palsy, J. Bone Joint Surg. Br. 85 (March (2)) (2003) 157–166. [4] T.A. Damron, T.A. Greenwald, A.L. Breed, Chronologic outcome of surgical tendoachilles lengthening and natural history of gastroc-soleus contracture in cerebral palsy. A two-part study, Clin. Orthop. Relat. Res. 301 (April) (1994) 249–255. [5] D.C. Borton, K. Walker, M. Pirpiris, G.R. Nattrass, H.K. Graham, Isolated calf lengthening in cerebral palsy. Outcome analysis of risk factors, J. Bone Joint Surg. Br. 83 (April (3)) (2001) 364–370. [6] A.H. Pierrot, O.B. Murphy, Albert E. Klinkicht Award, 1972. Heel cord advancement. A new approach to the spastic equinus deformity, Orthop. Clin. North Am. 5 (1) (1974) 117–126. [7] G.E. Fulford, Surgical management of ankle and foot deformities in cerebral palsy, Clin. Orthop. Relat. Res. 253 (April) (1990) 55–61. [8] J.J. Craig, J. van Vuren, The importance of gastrocnemius recession in the correction of equinus deformity in cerebral palsy, J. Bone Joint Surg. Br. 58 (March (1)) (1976) 84–87. [9] J.P. Lin, J.K. Brown, Peripheral and central mechanisms of hindfoot equinus in childhood hemiplegia, Dev. Med. Child Neurol. 34 (November (11)) (1992) 949–965. [10] D.C. Bland, L.A. Prosser, L.A. Bellini, K.E. Alter, D.L. Damiano, Tibialis anterior architecture, strength, and gait in individuals with cerebral palsy, Muscle Nerve 44 (4) (2011) 509–517. [11] R. Brunner, Muscle physiology and the effect of muscle-tendon surgery in cerebral palsy, Der Orthopäde 33 (October (10)) (2004) 1096–1102. [12] M. Mockford, J.M. Caulton, The pathophysiological basis of weakness in children with cerebral palsy, Paediatr. Phys. Ther. 22 (2) (2010) 222–233.
27
[13] E. Rutz, R. Baker, O. Tirosh, J. Romkes, C. Haase, R. Brunner, Tibialis anterior tendon shortening in combination with Achilles tendon lengthening in spastic equinus in cerebral palsy, Gait Posture 33 (February (2)) (2011) 152–157. [14] R. Baker, J.L. McGinley, M.H. Schwartz, S. Beynon, A. Rozumalski, H.K. Graham, et al., The gait profile score and movement analysis profile, Gait Posture 30 (October (3)) (2009) 265–269. [15] H.S. Read, M.E. Hazlewood, S.J. Hillman, R.J. Prescott, J.E. Robb, Edinburgh visual gait score for use in cerebral palsy, J. Pediatr. Orthop. 23 (January (3)) (2016) 296–301. [16] A.M.L. Ong, S.J. Hillman, J.E. Robb, Reliability and validity of the Edinburgh Visual Gait Score for cerebral palsy when used by inexperienced observers, Gait Posture 28 (August (2)) (2008) 323–326. [17] S.J. Hillman, M.E. Hazlewood, M.H. Schwartz, M.L. van der Linden, J.E. Robb, Correlation of the Edinburgh Gait Score with the Gillette Gait Index, the Gillette Functional Assessment Questionnaire, and dimensionless speed, J. Pediatr. Orthop. 27 (January (1)) (2016) 7–11. [18] C. Rathinam, A. Bateman, J. Peirson, J. Skinner, Observational gait assessment tools in paediatrics—a systematic review, Gait Posture 40 (June (2)) (2014) 279–285. [19] L.W. Robinson, N. Clement, M. Fullarton, A. Richardson, J. Herman, G. Henderson, et al., The relationship between the Edinburgh Visual Gait Score, the Gait Profile Score and GMFCS levels I-III, Gait Posture 41 (February (2)) (2015) 741–743. [20] R.W. Bohannon, M.B. Smith, Interrater reliability of a modified Ashworth scale of muscle spasticity, Phys. Ther. 67 (February (2)) (1987) 206–207. [21] J.R. Mendell, J. Florence, Manual muscle testing, Muscle Nerve 13 (January (Suppl. S16–20)) (1990). [22] S.C. Cuthbert, G.J. Goodheart, On the reliability and validity of manual muscle testing: a literature review, Chiropr. Osteopat. 15 (January) (2007) 4.A. [23] M.P. Kadaba, H.K. Ramakrishnan, M.E. Wootten, Measurement of lower extremity kinematics during level walking, J. Orthop. Res. 8 (May (3)) (1990) 383–392. [24] S. Gupta, K. Raja, Responsiveness of Edinburgh Visual Gait Score to orthopedic surgical intervention of the lower limbs in children with cerebral palsy, Am. J. Phys. Med. Rehabil. 91 (October (9)) (2012) 761–767. [25] D.E. Rassier, B.R. MacIntosh, W. Herzog, Length dependence of active force production in skeletal muscle, J. Appl. Physiol. 86 (May 1 (5)) (1999) 1445–1457. [26] S. Levitt, The Pathophysiological Basis of Weakness in Children With Cerebral Palsy, 5th ed., Wiley-Blackwell, Oxford: Malden, Mass, 2010 356 p.. [27] D.B. Lotman, Knee flexion deformity and patella alta in spastic cerebral palsy, Dev. Med. Child Neurol. 18 (June (3)) (1976) 315–319. [28] R.K. Beals, Treatment of knee contracture in cerebral palsy by hamstring lengthening, posterior capsulotomy, and quadriceps mechanism shortening, Dev. Med. Child Neurol. 43 (February 13 (12)) (2007) 802–805. [29] L.A.B. Ferreira, V. Cimolin, P.F. Costici, G. Albertini, C.S. Oliveira, M. Galli, Effects of gastrocnemius fascia lengthening on gait pattern in children with cerebral palsy using the gait profile score, Res. Dev. Disabil. 35 (2014) 1137–1143. [30] S. Ounpuu, M. Solomito, K. Bell, P. DeLuca, K. Pierz, Long-term outcomes after multilevel surgery including rectus femoris, hamstring and gastrocnemius procedures in children with cerebral palsy, Gait Posture 42 (2015) 365–372.