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1. Introduction and literature review

1.5. Pathology on muscle-tendon level in Cerebral Palsy

1.5.2. Macroscopic alterations

1.5.2.1. Fascicle propertie

A B

Fig. 1-10 Section of a cadaver medial gastrocnemius and in-vivo ultrasound picture. A) Anatomical section of a cadaver muscle belly. Extracted from Bernard et al., 2009, Muscle Nerve 39, 652-665, p.657. With permission from John, Wiley and Sons. B) 2D in-vivo ultrasound scan of the medial gastrocnemius muscle belly. Ultrasound picture with schematic drawings of a fascicle and its pennation angle from own measurements. Scale unit=1cm.

The associated graphic of the shank was extracted and adapted from Kawakami and Fukunaga, 2006, Exerc Sport

Numerous studies used ultrasonography to evaluate muscle structure by making use of the fact that connective tissue can be discriminated from active muscle tissue (Cronin and Lichtward, 2013).

Amongst others, fascicle (~fibre bundle) length and their orientation can be determined (Fig. 1-10).

Since muscle fibres may not span the entire width or length of muscles, it had been suggested that fascicle and fibre should not be used as synonyms. Since most fibres seem to be serially connected, fascicles are considered the ‘functional unit’ for representing fibres (Kumagai et al., 2000). In terms of gastrocnemius fascicles, cadaveric studies suggest that the error between actual fibre bundle length (Fig. 1-10) and fascicle length from 2D ultrasound can be minimized by following specific protocols for ultrasound probe orientation (Benard et al., 2011). In terms of validity, the anatomical accuracy of measurements of fascicle lengths and pennation angles revealed a standard error of 8.7–9.7% (Kwah et al., 2013). Concerning brightness-mode ultrasonography of the medial gastrocnemius, acceptable reproducibility during passive assessments has been established in children with CP (Mohagheghi et al., 2007), as well as in typically developing children (Legerlotz et al., 2010). In CP children, ICC values of 0.81-0.91, 0.85-0.88 and 0.93-0.94 have been established for fascicle length, pennation angle and muscle belly thickness, respectively (Mohagheghi et al., 2007). The average difference between repeated measures was ≤8.1% for fascicle length and ≤8% for muscle belly thickness while it was 2-3°

for pennation angles. For healthy controls, Legerlotz et al. (2010) found somewhat larger ICC values and lower coefficients of variation: <6.3% for fascicle length and <3.1% for muscle belly thickness.

As depicted in Fig. 1-11, longer muscle fascicles (with more sarcomeres in series) can be beneficial for various reasons: They may extend the range for active force production (O'Brien, 2016), they are able to produce higher shortening velocities (Blazevich and Sharp, 2005) and they exert higher forces closer to their maximum across a wider range (O'Brien, 2016). Since relative shortening is less, relative contractile velocity is lower in long fascicles and this enables the production of larger forces. Moreover, additional sarcomeres in series may also increase passive muscle extensibility (Butterfield, 2010). They may speculatively also have a protective effect for the muscle by shifting its optimum length to avoid eccentric contractions beyond optimum (Morgan and Proske, 2004). On the other hand, there might also be a tradeoff since longer fascicles can increase the cost for generating force, since more sarcomeres need to be activated (Lichtwark and Wilson, 2008).

Fig. 1-11 Benefits of larger PCSA and longer muscle fibres on force-length and force-velocity relationship.

Schematic illustration. Extracted and adapted from Lieber and Fridén, 2000, Muscle Nerve 23, 1647-1666, p.1659 and p.1660. With permission from John Wiley & Sons.

In healthy adults, longer gastrocnemius fascicles have been positively associated with sprinters and their performance (Abe et al., 2000; Kumagai et al., 2000). Furthermore, Hauraix et al. (2015) experimentally confirmed that, in vivo, the maximum concentric gastrocnemius fascicle force in humans is a function of its shortening velocity.

Contrarily, bed-rest immobilization (Boer et al., 2008), aging (Narici et al., 2003; Stenroth et al., 2012; Thom et al., 2007) as well as neurological insults, e.g. stroke (Gao et al., 2009) have been reported to negatively affect gastrocnemius architecture and reduce fascicle length. Interestingly, in older aged individuals, decreased fascicle length accounts for half of the age related decline of maximal muscle shortening velocity (Thom et al., 2007). In adult stroke survivors, associations between reduced gastrocnemius fascicle length and restrictions in passive joint motion, as well as increased joint stiffness have been found (Gao et al., 2009).

In patients with CP, Barrett and Lichtwark (2010) concluded that there was no consistent evidence that plantarflexor fascicle length is reduced. Lack of standardization may provide a potential bias since most studies did not exactly standardize the joint configurations or the applied ankle moment during their assessments. Since Barrett and Lichtwark’s Review (2010), these discrepancies seemed to continue. Concerning the gastrocnemius, two further novel studies in CP children beyond 6 years of age confirm the notion that there is no difference in fascicle length (Barber et al., 2011b; Herskind et al., 2016). Yet, more standardized studies in older children (average age 11-13 years) found that within a common passive ankle range of motion, gastrocnemius fascicles of children with CP are considerably

reduced (-20% to -43%) with respect to typically developing peers (Gao et al., 2011; Kalkman et al., 2016; Matthiasdottir et al., 2014). A plausible explanation for the shorter fascicles may be a loss of serial sarcomeres as speculated by Matthiasdottir et al. (2014). Absolute passive extensibility (~strain) of the gastrocnemius fascicles was reported to be lower in children with CP (Barber et al., 2011a;

Kalkman et al., 2016). To the contrary, when considered over a common range of joint motion, the fascicles of CP children according to Matthiasdottir et al. (2014) undergo a bigger relative excursion as they are inherently shorter. Thus the authors speculated that each sarcomere within the gastrocnemius fascicles of children with CP is exposed to a greater mechanical demand upon stretch.

In summary, there is emerging evidence that fascicle length in the gastrocnemius of more mature children and adolescents with CP is reduced.