Muscle architectural changes after massive human rotator cuff tear

Abstract

Rotator cuff (RC) tendon tears lead to negative structural and functional changes in the associated musculature. The structural features of muscle that predict function are termed “muscle architecture”. Although the architectural features of “normal” rotator cuff muscles are known, they are poorly understood in the context of cuff pathology. The purpose of this study was to investigate the effects of tear and repair on RC muscle architecture. To this end thirty cadaveric shoulders were grouped into one of four categories based on tear magnitude: Intact, Full-thickness tear (FTT), Massive tear (MT), or Intervention if sutures or hardware were present, and key parameters of muscle architecture were measured. We found that muscle mass and fiber length decreased proportionally with tear size, with significant differences between all groups. Conversely, sarcomere number was reduced in both FTT and MT with no significant difference between these two groups, in large part because sarcomere length was significantly reduced in MT but not FTT. The loss of muscle mass in FTT is due, in part, to subtraction of serial sarcomeres, which may help preserve sarcomere length. This indicates that function in FTT may be impaired, but there is some remaining mechanical loading to maintain “normal” sarcomere length-tension relationships. However, the changes resulting from MT suggest more severe limitations in force-generating capacity because sarcomere length-tension relationships are no longer normal. The architectural deficits observed in MT muscles may indicate deeper deficiencies in muscle adaptability to length change, which could negatively impact RC function despite successful anatomical repair.

The role of mechanobiology in progression of rotator cuff muscle atrophy and degeneration

“…Suprascapular nerve dysfunction may also impact muscle remodeling, though the prevalence of neuropathy in RC tears appears to be limited . As the muscle retracts, muscle fibers shorten via serial sarcomere subtraction and the muscle becomes fibrotic (discussed in further detail below). This causes the working range of the muscle to decrease, and it has been hypothesized to increase RC muscles’ susceptibility to injury during repair given the high muscle tension and strain required to repair the retracted tendon to its footprint …”

“…While fibrosis predicts stiffness to a degree, the existing data suggests that muscle stiffness is dictated by additional variables. One possible contributor is reduced sarcomere number following tear, which would lead to higher average sarcomere strains for a given change in muscle length . Another possibility is that ECM modification, and not just content, dictate total ECM stiffness (and cell‐ECM interactions).…”

“…In parallel with alterations at the whole muscle level, individual muscle fibers undergo several detrimental changes as a result of chronic unloading, with distinct stages across the disease spectrum. In terms of muscle architecture, muscle fibers in full‐thickness tears have decreased sarcomeric order and increased accumulation of small (<1 μm) intracellular lipid droplets, but normal sarcomere length is maintained via serial sarcomere subtraction . However, in large or massive (>5 cm retraction) RC tears, normal sarcomere remodeling is not observed, and sarcomeres are significantly shorter than in either intact or full thickness tears .…”

“…However, in large or massive (>5 cm retraction) RC tears, normal sarcomere remodeling is not observed, and sarcomeres are significantly shorter than in either intact or full thickness tears . The implications of these findings are two‐fold: First, this suggest that muscle with moderate tears are more likely than larger tears to remodel and remain functional after repair, and second, that repair of massive tears may fail due to a combination of over‐strained sarcomeres immediately after repair and failure to adapt sarcomere length over time …”

“…In terms of surgical intervention and repair, the altered muscle architecture and increased stiffness must be considered, particularly in chronic, massive tears . These pathological changes suggest that repair of large tears may be futile from a functional standpoint, as repair may cause more damage and the muscle may not adapt sarcomere number and length normally . Tendon repair alone is also unlikely to ameliorate the pro‐degenerative/anti‐regenerative environment of the chronically torn cuff, further diminishing the likelihood of successful functional restoration in large and massive tears.…”