Analysis of Running Gait in Children with Cerebral Palsy: Barefoot vs. a New Ankle Foot Orthosis

unning is an essential activity for children with cerebral palsy (CP). This study aims to characterize the locomotor pattern of running in hemiplegic children with new generation ankle foot orthosis (AFOs) conceived to foster intense motor activities such as running. A group of 18 children with spastic hemiplegia was recruited. A biomechanical multivariable comparison was made between barefoot and with AFO running trials. The focus was devoted to bilateral sagittal plane hip, knee, ankle kinematics and kinetics, and three-dimensional ground reaction forces. Wearing the orthoses, the children were found to reduce cadence and the duration of the stance phase as well as increase the step and stride length. The new AFO resulted in signi cant changes in kinematics of affected ankle both at initial contact 0–3% GC (p< 0.017)

sagittal plane hip, knee, ankle kinematics and kinetics, and three-dimensional ground reaction forces. Wearing the orthoses, the children were found to reduce cadence and the duration of the stance phase as well as increase the step and stride length. The new AFO resulted in signi cant changes in kinematics of affected ankle both at initial contact 0–3% GC (p< 0.017) and during the entire swing phase 31–100%GC (p< 0.001) being the ankle more dorsi exed with AFO compared to barefoot condition. Ankle power was found to differ signi cantly both in absorption and generation 5–10%GC (p< 0.001); 21–27%GC (p< 0.001) with a reduction in both cases when the AFO was worn. No statistical differences were recorded in the GRF components, in the affected ankle torque and hip and knee kinematics and kinetics. Keywords:running; cerebral palsy; AFO; children; ankle foot orthosis; hemiplegia; sports 1. Introduction Running is the ability to generate a ight phase consistently between alternating foot strikes [1]. Running is an essential activity in a child's physical development, both for typically developing (TD) children and for children with pre-existing conditions such as cerebral palsy (CP) [2]. It is also crucial for social interactions since many recreational activities require the execution of this motor activity [3]. Children with CP of GMFCS level I and II (GMFCS: Gross Motor Function Classi ca- tion System) [4] are usually prescribed ankle foot orthoses (AFO) to facilitate locomotion. The current use of AFO is usually limited to the walking gait, excluding higher impact ac- tivities such as running and jumping [5]. It is well documented that the majority of children with cerebral palsy GMFCS level I-II are able to perform running activities [2,6–15]. Previ- ous studies stated that considering a group of 72 children with unilateral CP, 67% are able to run, but the dynamic balance requirements of running still remain challenging for about 33% of them [16,17]. In this context, the development of custom-made orthotic devices, such as AFOs, may be critical to facilitate running activities while reducing energy cost. If compared to walking, running requires greater involvement of the musculoskeletal system [2,18,19],

with unilateral CP, 67% are able to run, but the dynamic balance requirements of running still remain challenging for about 33% of them [16,17]. In this context, the development of custom-made orthotic devices, such as AFOs, may be critical to facilitate running activities while reducing energy cost. If compared to walking, running requires greater involvement of the musculoskeletal system [2,18,19], often de cient in children affected by neuromuscular diseases. In particu- lar, the most involved muscles in running propulsion are the hip exors and extensors, hip adductors, knee extensors, and ankle plantar exors [2,19,20]. The latter are often affected by spasticity, reducing propulsive force application in the limited stance time of running Int. J. Environ. Res. Public Health2022,19, 14203.

Int. J. Environ. Res. Public Health2022,19, 14203 2 of 10 with a consequent reduction in speed [6,21]. AFO designed for sports activities can help overcome these limitations. There are different types of AFOs (Figure), such as stabilization or proprioceptive type (also known as wDAFO or TRAFO), custom-made, or involving predisposed compo- nents. The most common among the stabilization AFOs is the solid AFO (sAFO), typically used in presence of a support equinism.Int. J. Environ. Res. Public Health 2022, 19, 14203 3 of 12 Figure 1. (A) solid ankle foot orthosis (sAFO), (B) ground reaction AFO (GRAFO), (C) hinged AFO (hAFO) (D) posterior leaf spring AFO (PLS), (E) carbon modular orthosis (CaMO). 2. Materials and Methods 2.1. Orthosis Type The new AFO belongs to the PLS group, and it is able to result in a greater elasticity than traditional PLS orthoses. This is made possible by combined use of a posterior carbon fiber composite leaf spring, polypropylene, and geometry specifically designed for sports practices. It is featured by a posterior opening to the sandal and a heel cushion made of shock-absorbing material to allow the adipose tissue of the heel expanding during the contact with the ground. In this way, it is possible to absorb the axial stress without traumatizing the lower limb. New AFO is an evolution of the Carbon Modular Orthosis (Ca.M.O) [31] an orthoprosthetic custom-made device patented by ITOP (no. Patent: 0001411806), whose peculiarities lie in the combination of different materials, modularity, and proper design of the structural elements (carbon leaf spring, sandal, and calf socket). In this study, the new AFO designed in accordance with anthropometric data (foot length, weight, distance between the heel apex, and popliteal fossa) [31] was provided to each child. A pair of orthopaedic shoes for neurological disorders of the same type (they only differ in size and color) manufactured by Duna (Falconara Marittina, Ancona, Italy) were also provided. 2.2. Study Design The research received approval from the ethics committee of the institute “IRCCS Eugenio Medea—Sezione Scientifica Associazione La Nostra Famiglia” and was performed according to the ethical principles set out in the

orthopaedic shoes for neurological disorders of the same type (they only differ in size and color) manufactured by Duna (Falconara Marittina, Ancona, Italy) were also provided. 2.2. Study Design The research received approval from the ethics committee of the institute “IRCCS Eugenio Medea—Sezione Scientifica Associazione La Nostra Famiglia” and was performed according to the ethical principles set out in the Declaration of Helsinki. All children’s parents or guardians read and signed the informed consent. Eighteen children with spastic hemiplegia (11 males and 7 females, age: 8.0 ± 1.5 years; weight: 27.4 ± 5.3 kg; height: 129.3 ± 7.3 cm) were recruited for this study (Table 1). The inclusion criteria were as follows: (1) a diagnosis of CP with hemiplegia or limitation prevalent to a lower limb; (2) age between 6 and 11 years; (3) users of AFO orthoses without any time limit; (4) GMFCS level I and II; and (5) Modified Ashworth score [32] less than or equal to 3 on the following muscles groups: triceps surae, hamstrings, and rectus femoris. Figure 1. (A) solid ankle foot orthosis (sAFO), (B) ground reaction AFO (GRAFO), (C) hinged AFO (hAFO) (D) posterior leaf spring AFO (PLS), (E) carbon modular orthosis (CaMO). Variants of the sAFO with an anterior socket, called ground reaction AFOs (GRAFO) or spiral AFOs, are mainly used in cases of crouch gait. The hinged AFOs (hAFO) may allow to limit and/or elastically control plantar exion and dorsi exion. Posterior leaf spring (PLS) orthoses, made of either thermoplastic or carbon fiber/kevlar/ berglass, facilitate dynamic element during the propulsive phase of the stride. Despite the variety of AFOs available on the market, the prescription of use is lim- ited to gait only, excluding running. Con rming this, even in the state-of-the-art, only several systematic reviews showed the use of AFOs in children with CP solely during walking [22–24]. In these studies, sAFOs and hAFOs were compared with barefoot walking, showing an improvement in initial contact, by reducing excessive equinus, and midstance. In addition, it was found that the ankle peak during dorsi exion was greater while the ankle peak power generation

only several systematic reviews showed the use of AFOs in children with CP solely during walking [22–24]. In these studies, sAFOs and hAFOs were compared with barefoot walking, showing an improvement in initial contact, by reducing excessive equinus, and midstance. In addition, it was found that the ankle peak during dorsi exion was greater while the ankle peak power generation and absorption decreased when wearing sAFO, hAFO, TRAFO, and PLS [15]. Pelvis, hip, and knee kinematics did not change when wearing sAFO, hAFO, and PLS. Stride and step length, gait velocity, and single support time increased whereas cadence decreased with sAFO, hAFO, and DAFO when compared to barefoot. According to Lintanf et al. [23], no extensive study on running of children with cerebral palsy wearing orthotic aids was led, both from a kinematic and dynamic point of view. As stated by Gibson et al. and Chappell et al. [2,25], only few authors including Krätschmer [26], Davis [14], Bohm and Doderlein [8], Kloyia, M. [27] and Iosa [7] have analyzed kinematics and/or kinetics dynamics of barefoot and shoed running in hemiplegic and diplegic children, while Russell investigated the orthoses effect on running on a group of highly trained soldiers [28–30]. These previous studies showed that it is possible to modify the locomotor running pattern by moving from rearfoot strike to forefoot initial contact, improving mechanical performance. This study aims to test a new generation AFO designed to foster bene cial running biomechanical changes in children with CP. The locomotor pattern of running in hemi- plegic children has been fully characterized. Speci cally, a biomechanical multivariable comparison between barefoot and AFO trials was performed considering hip, knee, ankle joint kinematics and kinetics in the sagittal plane, and the three ground reaction force (GRF) components. 2. Materials and Methods 2.1. Orthosis Type The new AFO belongs to the PLS group, and it is able to result in a greater elasticity than traditional PLS orthoses. This is made possible by combined use of a posterior carbon

(GRF) components. 2. Materials and Methods 2.1. Orthosis Type The new AFO belongs to the PLS group, and it is able to result in a greater elasticity than traditional PLS orthoses. This is made possible by combined use of a posterior carbon

Int. J. Environ. Res. Public Health2022,19, 14203 3 of 10 ber composite leaf spring, polypropylene, and geometry speci cally designed for sports practices. It is featured by a posterior opening to the sandal and a heel cushion made of shock-absorbing material to allow the adipose tissue of the heel expanding during the contact with the ground. In this way, it is possible to absorb the axial stress without traumatizing the lower limb. New AFO is an evolution of the Carbon Modular Orthosis (Ca.M.O) [31] an orthopros- thetic custom-made device patented by ITOP (no. Patent: 0001411806), whose peculiarities lie in the combination of different materials, modularity, and proper design of the structural elements (carbon leaf spring, sandal, and calf socket). In this study, the new AFO designed in accordance with anthropometric data (foot length, weight, distance between the heel apex, and popliteal fossa) [31] was provided to each child. A pair of orthopaedic shoes for neurological disorders of the same type (they only differ in size and color) manufactured by Duna (Falconara Marittina, Ancona, Italy) were also provided. 2.2. Study Design The research received approval from the ethics committee of the institute “IRCCS Eugenio Medea—Sezione Scienti ca Associazione La Nostra Famiglia” and was performed according to the ethical principles set out in the Declaration of Helsinki. All children's parents or guardians read and signed the informed consent. Eighteen children with spastic hemiplegia (11 males and 7 females, age:8.0 1.5 years; weight: 27.4 5.3 kg; height: 129.3 7.3 cm) were recruited for this study (Table). The inclusion criteria were as follows: (1) a diagnosis of CP with hemiplegia or limitation prevalent to a lower limb; (2) age between 6 and 11 years; (3) users of AFO orthoses without any time limit; (4) GMFCS level I and II; and (5) Modi ed Ashworth score [32] less than or equal to 3 on the following muscles groups: triceps surae, hamstrings, and rectus femoris. Table 1. Participants characteristics. They were classi ed according to gender, age, weight, height, diagnosis, and GMFCS (Gross Motor Function Classi cation System). ID Sex Age (Years) Weight (kg) Height (cm)

GMFCS level I and II; and (5) Modi ed Ashworth score [32] less than or equal to 3 on the following muscles groups: triceps surae, hamstrings, and rectus femoris. Table 1. Participants characteristics. They were classi ed according to gender, age, weight, height, diagnosis, and GMFCS (Gross Motor Function Classi cation System). ID Sex Age (Years) Weight (kg) Height (cm) Diagnosis GMFCS 1 M 9 27.5 137.5 Hemi R II 2 F 10 39 143 Hemi L I 3 M 10 23 130 Hemi R II 4 M 6 23 119 Hemi R II 5 M 10 32.5 140 Hemi R I 6 M 10 33 129 Hemi R I 7 F 7 23 116.5 Hemi R II 8 M 7 27 135.5 Hemi R II 9 F 8 31 136.5 Hemi L I 10 M 8 24 129 Hemi L II 11 F 7 29 129 Hemi R I 12 M 10 21.5 130 Hemi L II 13 M 8 23 124.5 Hemi L I 14 F 8 37.5 132 Hemi R II 15 M 7 25 126 Hemi R I 16 M 7 28 125 Hemi L II 17 F 5 24 125 Hemi L I 18 F 7 22 120 Hemi L II Mean (SD) [M: F] 11: 7 8.0 (1.5) 27.4 (5.3) 129.3 (7.3) [R: L] 10: 8 [I: II] 8: 10 Children using knee and hip tract orthoses (KAFO, HKAFO), having assisted walking needs (use of crutches, walkers, or other), or being uncooperative were not involved inthe study. Data were collected in the gait analysis laboratory “ASTROLAB” IRCCS Eugenio Medea (Associazione La Nostra Famiglia, Bosisio Parini, Lecco, Italy) equipped with eight-

Int. J. Environ. Res. Public Health2022,19, 14203 4 of 10 camera optoelectronic system (BTS Smart DX 700 Bioengineering, Milano, Italy) and four coupled force platforms (BTS P-6000, Bioengineering, Milano, Italy). Twenty-six passive re ective markers were placed following Davis protocol [33,34]. Speci cally, the lower limb segments (pelvis, thighs, shanks, and feet) were used. The trials were performed in two conditions: (1) barefoot running and (2) AFO + orthopaedic shoes running after about 30 days of acclimatization period. During tests involving orthopaedic shoes, foot segment markers were placed on the shoe by reproducing as accurately as possible the heel and fifth metatarsal anatomical landmarks. Each participant was verbally instructed to run along a straight trajectory of about 12 m from a starting point to a nishing point identi ed by eld delimiters. No indications on running speed or foot impact with the force platforms were given. Due to space constraints, the approach length was 2 m, and the additional distance before and after the region of data collection was 1 m. A suf cient number of trials was performed to have a valid trial in which the child places at least one foot on the force platforms. 2.3. Studied Variables The spatio-temporal parameters, the ground reaction forces (GRFs), and the kinetic and the kinematic variables at the hip, knee, and ankle joint in the sagittal plane were obtained using a protocol implemented in SMART Analyzer (BTS Bioengineering, Milano, Italy) and post-processed in an ad hoc Matlab ® script (MathWorks, Inc., Natick, MA, USA). Once the time instants of initial and final foot contact with the ground were defined, the kinetic and the kinematic data were time normalized to 100 samples and the run cycle with a free float phase was determined in the same way as the gait cycle (%GC). The GRFs were time normalized with respect to the stance phase (i.e., between the contact of one foot on the force platform and the toe off of the same foot). Data from both lower limbs were analyzed to have a valid trial for the more and less affected side. The

determined in the same way as the gait cycle (%GC). The GRFs were time normalized with respect to the stance phase (i.e., between the contact of one foot on the force platform and the toe off of the same foot). Data from both lower limbs were analyzed to have a valid trial for the more and less affected side. The classifications of the more affected and less affected side were defined with reference to the plegic side shown in Table considered valid only one trial per child. In case the entire stride for each side was not available in a single trial, one trial per each side (the affected and the unaffected one) was analyzed. 2.4. Statistics The statistical analysis was performed through one dimensional statistical parametrical mapping (SPM), using an open-source code ( ® environ- ment (version R2020a) that uses random field theory to make statistical inferences regarding registered (normalized) sets of 1D measurements [35]. The method is able to identify clusters in the running cycle where the compared variables differ statistically from each other. After testing the normality of the data using the function “spm1d.stats.normality.ttest”, a two- tailed pairedt-test with Bonferroni correction with a level of significance = 0.01 (function “spm1d.stats.ttest_paired” implemented in Matlab ® environment) was used to compare the two conditions of the trials (barefoot vs AFO). Overall, seven gait cycle variables (Table twelve kinematic and kinetic variables were statistically tested (Figures Table 2. Mean and standard deviation (M SD) of seven spatio-temporal parameters. Pairedt-test with Bonferroni correctionp< 0.010. + values for the affected side. GC: gait cycle. Variables Barefoot Orthosis p-Value speed (m/s) 2.9 0.5 3.0 0.5 0.120 cadence (step/min) 220.1 0.5 200.4 28.8 <0.010 step width (m) 0.11 0.04 0.10 0.05 0.750 stride length (m) + 1.54 0.21 1.75 0.28 <0.010 step length (m) + 0.77 0.10 0.86 0.13 <0.010 stance (% GC) + 34.7 4.4 31.3 6.2 <0.010 swing (%GC) + 65.3 4.4 68.7 6.2 <0.010

(m) + 1.54 0.21 1.75 0.28 <0.010 step length (m) + 0.77 0.10 0.86 0.13 <0.010 stance (% GC) + 34.7 4.4 31.3 6.2 <0.010 swing (%GC) + 65.3 4.4 68.7 6.2 <0.010

This study compares running gait in children with CP using AFOs versus barefoot.