Causes and consequences of equinus gait

The function of plantarflexors during walking is to control tibia advancement, supply propulsion and, in the case of gastrocnemius, accelerate the forward swinging leg (Arnold et al., 2005; Neptune et al., 2001). Further, plantarflexors also contribute to a more upright gait, e.g. the soleus controls tibia advancement and indirectly affects knee extension (Arnold et al., 2005) while both the soleus and the gastrocnemius were shown to provide vertical center of mass accelerations (Steele et al., 2013).

Children with SCP often walk in equinus which means that they contact the ground with the fore- or midfoot and lack dorsiflexion excursion. Experts assume that the gastrocnemius is generally more involved in equinus pathologies (Sees and Miller, 2013). Equinus gait affects 63-64% of the children classified in Gross Motor Function Classification System (GMFCS) Level I and II (Rethlefsen et al., 2016).

The lack of dorsiflexion in swing supposedly increases the risk of tripping while the limited base of support during stance may impair balance (Goldstein and Harper, 2001). The consequences are not locally limited to the ankle joint: Concerning the knee, excessive flexion (48-61% prevalence) or hyperextension in stance may be related (20% prevalence). During swing, 41-60% display an additional lack of kneeflexion (Rethlefsen et al., 2016). Additionally, children with equinus are at risk for

developing complex bony foot deformities and 5-24% of children in GMFCS I-II develop valgus feet with a sagged midfoot (Rethlefsen et al., 2016).

Equinus gait usually gets less prominent in older children with CP since young tip-toe walkers, primarily children classified in GMFCS I (Rethlefsen et al., 2016) and bilaterally affected children (Wren et al., 2005) seem to be prone to walk with increased knee flexion later in life (Rethlefsen et al., 2016;

Sees and Miller, 2013). Thus, a reduced equinus posture during gait may not indicate that the underlying muscle dysfunction or contracture of the calf has been resolved. Quite the contrary, a progressive reduction of passive dorsiflexion is often over time related to more knee flexion during gait (Maas et al., 2015). This is presumably caused by structural shortness of the bi-articular gastrocnemius. On the other hand, despite a loss in passive dorsiflexion, some CP children can also maintain adequate knee flexion during gait (Bell et al., 2002). Whether children sort of vertically collapse during gait is probably influenced by others factors such as plantarflexor weakness. Notably, also patients with idiopathic gastrocnemius tightness compensate their deficits either at the knee or at the ankle during walking (Chimera et al., 2012; You et al., 2009).

As stated at the beginning of this section, plantarflexors provide propulsion and thus reduced isometric plantarflexor strength of children with CP is associated with less ankle joint power generation while walking (Dallmeijer et al., 2011; Eek et al., 2011). In addition, it had been shown that both reduced ankle range of motion during gait and decreased ankle joint propulsion increases the energy expenditure index (relationship between heart rate and walking speed) during gait of CP children (Pouliot-Laforte et al., 2014).

Searching for the causes of equinus gait, it is assumed that an accentuated strength imbalance between hypertonic plantar- and weak dorsiflexors favors walking in equinus (Hof, 2001). However, the majority of studies report that on average the relative weakness in dorsiflexors is somewhat less pronounced than that of plantarflexors (Downing et al., 2009; Elder et al., 2003; Ross and Engsberg, 2002; Wiley and Damiano, 1998; Hussain et al., 2014) vs. (Poon and Hui-Chan, 2009).

In fact, it appears debatable whether equinus posturing during gait is a cause for functional weakness or an adaptive strategy. On the one hand, computer simulations suggest that toe walking requires more neural muscle activity due to non-optimal conditions concerning the plantarflexors’

muscle force-length relationship (Neptune et al., 2007). This may lead to premature fatigue.

Experiments on gait of typically developing children also suggest that there is a negative impact of equinus posture on plantarflexor force production: When artificially restricting dorsiflexion during gait (Houx et al., 2013) or when voluntarily walking in equinus (Davids et al., 1999), kinetic measures of ankle joint propulsion decline. On the other hand, instrumented strength tests show that the maximal plantarflexor force generating capacity of CP patients is shifted towards plantarflexion angles (Barber

strategy to provide adequate force output. Eventually, since ankle moments during walking exceed active moment generation during strength tests in children with CP (Dallmeijer et al., 2011; Eek et al., 2011), it was speculated that the loss in passive joint motion should be regarded as an adaptive mechanism in order to rely on passive structures to substitute for missing active strength.

Another cause for equinus gait could be neural dysfunction of spastic plantarflexors. This is quite a controversial topic: Prolonged or abnormally timed plantarflexor activity, as well as co-contraction with dorsiflexors are frequently considered attributes of disturbed neural control. Since young CP patients, often have more pronounced equinus posturing while walking than upon clinical examination, the dysfunction is thought to be dominated by disturbed neural control and not by contracture (Goldstein and Harper, 2001). This is also described as ‘dynamic equinus’ (Goldstein and Harper, 2001). Yet, this terminology is rather confusing: To distinguish dynamic from fixed equinus, typically a cut-off for passive dorsiflexion is chosen, e.g. max. 5° (Zwick et al., 2004) or neutral ankle alignment (Wren et al., 2010). This may ultimately need to be verified with the patient under anesthesia (Dreher et al., 2012). However the degree of contracture formation is probably difficult to judge. Since CP children show a lack of volumetric muscle growth of the gastrocnemius at a very early age (Barber et al., 2011b) (see 2.2.1) and since dorsiflexion seems to be progressively lost during maturation (Hägglund and Wagner, 2011), a continuum of pathological muscle structural changes appears more reasonable.

Furthermore, mimicry studies pointed out that EMG features during gait, such as premature gastrocnemius activity at the transitions from swing to stance phase, or co-activation of the tibialis anterior and gastrocnemius are representative for toe-walking per-se and not unique to equinus in CP (Davids et al., 1999). Besides, both children with CP and children who walk on their toes for non-neurological reasons display rather similarly altered timing of gastrocnemius and tibialis anterior activity during gait (Rose et al., 1999). Apart from timing issue, there is little knowledge about the role of exaggerated reflexes, however they are thought to be of minor disabling effect (Dietz and Sinkjaer, 2007). For example, concerning children with unilateral CP, Willerslev-Olsen et al. (2014a) showed that exaggerated soleus reflexes did not impede foot lift and further concluded that a reduced central drive to dorsiflexors might have a stronger effect on the landing pattern of the foot. –Still, neural dysfunction of plantarflexors might also be disabling since, for example, increased firing frequencies in the EMG signal of calf muscles of children with CP were reported (Lam et al., 2005; van Gestel et al., 2012). Also, there is preliminary evidence that this reflects muscle weakness (van Gestel et al., 2012). How this relates to equinus posturing is yet unknown.

In summary, a lack of passive dorsiflexion seems to have a detrimental influence on ankle and knee function during gait of children with CP, predisposes for developing foot disorders, and may contribute to a slower and inefficient gait pattern. Apart from structural shortening of the plantarflexor muscle-tendon units, the primary neurological dysfunction seems to be an impaired central drive for force production. Hyper excitability of plantarflexor reflexes during gait has not been directly proven to be dysfunctional. It appears plausible that equinus posturing may be predominantly a consequence of the biomechanical restrictions imposed by the musculoskeletal system and to a lesser extent affected by abnormal muscle activity.