Serial sarcomere number is substantially decreased within the paretic biceps brachii in individuals with chronic hemiparetic stroke

Abstract

A muscle’s structure, or architecture, is indicative of its function and is plastic; changes in input to or use of the muscle alter its architecture. Stroke-induced neural deficits substantially alter both input to and usage of individual muscles. We combined in vivo imaging methods (second-harmonic generation microendoscopy, extended field-of-view ultrasound, and fat-suppression MRI) to quantify functionally meaningful architecture parameters in the biceps brachii of both limbs of individuals with chronic hemiparetic stroke and in age-matched, unimpaired controls. Specifically, serial sarcomere number (SSN) and physiological cross-sectional area (PCSA) were calculated from data collected at three anatomical scales: sarcomere length, fascicle length, and muscle volume. The interlimb differences in SSN and PCSA were significantly larger for stroke participants than for participants without stroke (P = 0.0126 and P = 0.0042, respectively), suggesting we observed muscle adaptations associated with stroke rather than natural interlimb variability. The paretic biceps brachii had ∼8,200 fewer serial sarcomeres and ∼2 cm2 smaller PCSA on average than the contralateral limb (both P < 0.0001). This was manifested by substantially smaller muscle volumes (112 versus 163 cm3), significantly shorter fascicles (11.0 versus 14.0 cm; P < 0.0001), and comparable sarcomere lengths (3.55 versus 3.59 μm; P = 0.6151) between limbs. Most notably, this study provides direct evidence of the loss of serial sarcomeres in human muscle observed in a population with neural impairments that lead to disuse and chronically place the affected muscle at a shortened position. This adaptation is consistent with functional consequences (increased passive resistance to elbow extension) that would amplify already problematic, neurally driven motor impairments.

Effect of Stretching of Spastic Elbow Under Intelligent Control in Chronic Stroke Survivors—A Pilot Study

“…Spastic muscles have the tendency to affect the sarcomere length, leading to either their lengthening or shortening as compared to the optimum sarcomere length (49)(50)(51)(52). The stretching may have the potential to either increase the length of the spastic muscle or its tendon so that the abnormally lengthened or shortened sarcomeres could possibly regain some of their optimal length and help generate higher force capacity (21,50,(52)(53)(54).…”

Variability of in vivo Sarcomere Length Measures in the Upper Limb Obtained With Second Harmonic Generation Microendoscopy

“…As described previously ( Adkins et al, 2021 ), a spring loaded injector was used to insert the microendoscopic probe into the muscle. Once inserted, images are acquired 0.3 cm superficial to the tip of the probe.…”

“…Once the probe was placed as desired within the muscle belly, a second-harmonic generation microscope (Enspectra Health, Mountain View, CA, United States) was attached to it for imaging. In this implementation [probe design same as ( Lichtwark et al, 2018 ; Adkins et al, 2021 ) as opposed to older design ( Sanchez et al, 2015 ; Chen and Delp, 2016 ; Chen et al, 2016 )], laser light travels down one of the probe’s needles, interacts with the muscle tissue, and is then received by the other needle. The resulting images capture the intrinsic striation pattern (A-bands) of sarcomeres and have a field of view of 82 × 82 microns.…”

“…Current image processing methods for analysis of SHG images (mean sarcomere length code; MSLC) report a single mean sarcomere length value for an entire image (e.g., Sanchez et al, 2015 ; Adkins et al, 2021 ). Here, we developed and validated an image processing and analysis code (individual sarcomere length code: ISLC) which quantifies: the lengths of individual sarcomeres within an image, the mean length of these sarcomeres, and standard deviation in sarcomere length within the image.…”

“…Sarcomere length variability across different images from a single imaging trial (defined as a single needle insertion and microscope attachment) was assessed using the standard deviation of the mean sarcomere length from all processed images in the trial. For this study, we reanalyzed images originally collected for a separate study ( Adkins et al, 2021 ) that were acquired in the non-paretic biceps of 7 individuals with chronic hemiparetic stroke and in the biceps from both the dominant and non-dominant limbs of 4 individuals with no neuromuscular impairments ( Table 1 ). Therefore, SHG images were collected from the long head of the biceps brachii in 15 limbs.…”