Changes in muscle\u2013tendon unit length\u2013force characteristics following experimentally induced photothrombotic stroke cannot be explained by changes in muscle belly structure

Arjun Paudyal,Hans Degens,Erwin Van Wegen,Gert Kwakkel,Huub Maas,Wendy Noort,Guus C Baan,Mark Slevin

doi:10.1007/s00421-021-04729-x

Abstract

PurposeThe aim of this study was to assess the effects of experimentally induced photothrombotic stroke on structural and mechanical properties of rat m. flexor carpi ulnaris.MethodsTwo groups of Young-adult male Sprague–Dawley rats were measured: stroke (n = 9) and control (n = 7). Photothrombotic stroke was induced in the forelimb region of the primary sensorimotor cortex. Four weeks later, muscle–tendon unit and muscle belly length–force characteristics of the m. flexor carpi ulnaris, mechanical interaction with the neighbouring m. palmaris longus, the number of sarcomeres in series within muscle fibres, and the physiological cross-sectional area were measured.ResultsStroke resulted in higher force and stiffness of the m. flexor carpi ulnaris at optimum muscle–tendon unit length, but only for the passive conditions. Stroke did not alter the length–force characteristics of m. flexor carpi ulnaris muscle belly, morphological characteristics, and the extent of mechanical interaction with m. palmaris longus muscle.ConclusionThe higher passive force and passive stiffness at the muscle–tendon unit level in the absence of changes in structural and mechanical characteristics of the muscle belly indicates that the experimentally induced stroke resulted in an increased stiffness of the tendon.

Highlights

Stroke is the leading cause of disability and fourth leading cause of adult death; the number of people living with stroke in Europe is expected to increase by one million between 2015 and 2035, reaching 4,631,050 (Sacco et al 2013; Feigin et al 2017; Norrving et al 2018; GBD 2016 Neurology Collaborators 2019) Around 79% of patients suffering a stroke survive for at least 1 year (Radisauskas et al 2019), but the majority of survivors experience motor disabilities and sensorimotor deficits, including disrupted motor control and spasticity, which have a negative impact on the quality of life of stroke survivors (Burvill et al 1997; Langhorne et al 2011)
It has been observed in a rat model with spastic paresis that the muscle weakness is accompanied by a narrowing of the length–force relationship and an increased passive stiffness of the muscle–tendon unit (MTU) (Olesen et al 2014)
7 days after induction of stroke; this rat was not used for length–force assessment. c, e Tetrazolium Chloride (TTC) stained coronal sections of the brain 4 weeks after stroke from a representative rat tested for muscle mechanical properties

Summary

Introduction

Stroke is the leading cause of disability and fourth leading cause of adult death; the number of people living with stroke in Europe is expected to increase by one million between 2015 and 2035, reaching 4,631,050 (Sacco et al 2013; Feigin et al 2017; Norrving et al 2018; GBD 2016 Neurology Collaborators 2019) Around 79% of patients suffering a stroke survive for at least 1 year (Radisauskas et al 2019), but the majority of survivors experience motor disabilities and sensorimotor deficits, including disrupted motor control and spasticity, which have a negative impact on the quality of life of stroke survivors (Burvill et al 1997; Langhorne et al 2011).The motor disabilities are largely a consequence of muscle weakness due, at least transiently, to an impaired cortico- and reticulospinal control of muscles after a stroke (Patten et al 2004), that contribute to spasms (Bethoux 2015) and limited fascicle shortening (Son et al 2020). It has been observed in a rat model with spastic paresis that the muscle weakness is accompanied by a narrowing of the length–force relationship and an increased passive stiffness of the muscle–tendon unit (MTU) (Olesen et al 2014). It was suggested that this increased stiffness could, among other factors, be attributable to loss of number of sarcomeres in series, a situation seen in the paretic biceps brachii of stroke patients (Adkins et al 2020). This loss of sarcomeres in series is expected to cause a shift of the optimum length to shorter muscle and fascicle lengths. Spastic muscle fibres develop passive tension at shorter sarcomere length and have a higher elastic modulus compared to the normal muscle fibres (Fridén and Lieber 2003)

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