The role of the peripheral and central nervous systems in rotator cuff disease

doi:10.1016/j.jse.2015.04.004

Journal of Shoulder and Elbow Surgery

Volume 24, Issue 8, August 2015, Pages 1322-1335

https://doi.org/10.1016/j.jse.2015.04.004 Get rights and content

Rotator cuff (RC) disease is an extremely common condition associated with shoulder pain, reduced functional capacities, and impaired quality of life. It primarily involves alterations in tendon health and mechanical properties that can ultimately lead to tendon failure. RC tendon tears induce progressive muscle changes that have a negative impact on surgical reparability of the RC tendons and clinical outcomes. At the same time, a significant base of clinical data suggests a relatively weak relationship between RC integrity and clinical presentation, emphasizing the multifactorial aspects of RC disease. This review aims to summarize the potential contribution of peripheral, spinal, and supraspinal neural factors that may (1) exacerbate structural and functional muscle changes induced by tendon tear, (2) compromise the reversal of these changes during surgery and rehabilitation, (3) contribute to pain generation and persistence of pain, (4) impair shoulder function through reduced proprioception, kinematics, and muscle recruitment, and (5) help explain interindividual differences and response to treatment. Given the current clinical and scientific interest in peripheral nerve injury in the context of RC disease and surgery, we carefully reviewed this body of literature with a particular emphasis on suprascapular neuropathy that has generated a large number of studies in the past decade. Within this process, we highlight the gaps in current knowledge and suggest research avenues for scientists and clinicians.

Section snippets

Proprioceptors and related spinal reflexes

Shoulder movements and positional changes induce a deformation of tissues surrounding joints, including skin, muscles, tendons, fascia, joint capsules, and ligaments.24, 27, 47, 122, 144, 156 All these tissues are innervated by mechanically sensitive receptors termed proprioceptors that relay information to the central nervous system about movement, position, and forces exerted on shoulder structures (e.g., muscle spindles, Golgi tendon organs, Ruffini endings, Pacinian and Meissner

Central processing of proprioceptive information

Proprioceptive information from the shoulder and more broadly from the upper limb is conveyed through the spinothalamic tracts and relayed to the somatosensory cortex, where it is referred to a central body map allowing the conscious awareness of arm position and movement in space. Unconscious proprioceptive tracts (i.e., spinocerebellar tracts, projecting in the ipsilateral cerebellum) and the cervical propriospinal system are also involved in the coordination movements involving multiple

Nociceptors and peripheral and central pain processing

Nociceptors are high-threshold receptors that detect signals from damaged tissue or tissue on the verge of damage. They can be found in the shoulder, skin, muscles, joints, soft tissue, and bone.32, 40, 41, 51, 144, 149, 150 RC disease is associated with local tissue damage and inflammation within the RC and surrounding structures, which release a variety of substances that sensitize nociceptors by decreasing their activation threshold (peripheral sensitization), resulting in hyperalgesia at

Motor nerves and neuromuscular junction

The motor innervation of the RC muscles is achieved by nerves emerging from the posterior and the superior trunks of the brachial plexus, all originating from the C5-C6 cervical roots and C4 nerve root in some individuals.2, 81, 137, 167 The architecture and the high mobility of the shoulder complex predispose nerves to various dynamic or static compressive and traction injuries.¹⁴⁸ Cervical radiculopathy, brachial plexopathy, and peripheral nerve trunk injuries are potential comorbidities of

Sensory nerves

Sensory nerve injuries have received less interest than the motor neuropathies discussed before. However, the RC and surrounding structures receive sensory innervation from numerous sensory nerve branches29, 159 that are equally susceptible to injury. Injury within a peripheral nerve trunk induces a local inflammatory response that causes changes in afferent fibers and in the central nervous system and may lead to neurogenic pain (see section on nociceptors and peripheral and central pain

Shoulder muscle activity and kinematics

Alterations in shoulder muscle activity and kinematics of the glenohumeral and scapulothoracic joints have been widely reported in patients with RC disease.87, 97, 128 One potential contributing factor may be that patients with symptomatic tears display different motor control patterns during movement compared with asymptomatic patients.¹²⁸

Kelly et al⁷¹ observed that symptomatic patients retain supraspinatus and infraspinatus activity despite tendon tears but are unable to activate intact deep

Motor cortical changes

As in various other conditions, RC disease may induce structural and functional changes in the motor cortex that could partly explain changes in motor control and affect muscle activation. Little is known about the cortical organization of motoneurons related to proximal muscles of the arm and even less regarding RC muscles.¹⁰⁰ Functional magnetic resonance imaging has been previously used but is not discriminant for motor cortical mapping of individual RC muscles.⁷⁴ The output of the primary

Conclusion and perspective

In this review, we identified a large number of neural structures and mechanisms that may contribute to pain and shoulder dysfunction in patients with RC disease. These structures and mechanisms are summarized in Figure 1. However, numerous questions remain unanswered (Table II). Current data suggest that inflammation and muscle-tendon unit impairment disrupt proprioceptive function and reflex muscle activity. Alterations of proprioceptive afferents may impair proprioception and motor control,

Disclaimer

The authors, their immediate families, and any research foundation with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.

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Effectiveness of a joint mobilizations protocol for shoulder subacromial pain syndrome: A pilot study
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Subacromial pain syndrome (SPS) is the most frequent shoulder pathology. The aims of this prospective randomized study were to evaluate the effects of some specific shoulder joint mobilizations (“spin correction”), and the effectiveness of a rehabilitation program, named Shoulder Global Concept, in SPS patients.
45 patients with SPS were randomly assigned to two groups, to benefit from a different first session of mobilizations: the experimental group received all specific mobilizations, while the control group received the same program but without the spin correction mobilizations. The second session was identical for both groups, with all specific mobilizations. Before and after the first two sessions, range of motion (ROM) in flexion, abduction, external and internal rotations, pain and functional status with Constant score and Quick Dash were evaluated. Evaluation was repeated with 24 patients after 11 rehabilitation sessions. Rehabilitation with Shoulder Global Concept included 13 mobilizations aiming at improving the ROM with passive and active-assisted mobilizations, static stretching, and muscle strengthening.
All ROM were improved at the end of the first session for both groups, but significantly more in the experimental group for glenohumeral (GH) abduction and external rotation (p < 0.05). Functional scores, pain and strength were significantly improved after 11 rehabilitation sessions with the Shoulder Global Concept.
This manual therapy method was able to improve shoulder mobility in one session. The additional joint mobilizations (spin correction) specifically increased GH abduction and external rotation. Rehabilitation of SPS with Shoulder Global Concept allowed to improve functional capacity and decrease pain.
Peripheral neuropathies after shoulder arthroscopy: a systematic review
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Peripheral neuropathies after shoulder arthroscopy are rare, though likely under-reported. Many resolve spontaneously, but some patients are left with permanent neurological deficits. The purpose of this study was to review the literature to better characterize this patient population, diagnostic tests performed, the timing and type of surgical intervention, and report clinical outcomes.
A systematic literature review was performed. Articles in English were identified from PubMed, EMBASE, and CINAHL in August 2021. Article titles and abstracts were screened for relevance by two authors and discordant abstracts were resolved by the senior author. Data were subsequently extracted from the included articles.
Seventeen articles were identified yielding a total of 91 patients. The average age was 53 ± 12 years, and most patients were male (72%). Rotator cuff repair (62%) was the most common procedure performed. A peripheral neuropathy was identified an average of 80 ± 81 days from the index procedure (range, 0-240 days). Most commonly, peripheral nerve injury presented as a mononeuropathy, with the median nerve (39%) and ulnar nerve (17%) affected predominantly. Seventeen percent of patients underwent a secondary surgery at an average of 232 ± 157 days after the index procedure. At the final follow-up, 55% of neuropathies had resolved, 14% partially improved, and 22% showed no clinical improvement. The most proposed etiologies were postoperative immobilization (29%) and intraoperative positioning (20%), but several possible etiologies have been suggested.
Peripheral neuropathies after arthroscopic shoulder procedures are rare. While most spontaneously resolve, up to 1 in 5 patients may have persistent neuropathic symptoms. A high index of suspicion should be maintained throughout the postoperative period. When neurologic deficits are identified, patients should undergo a thorough diagnostic workup and be referred to a subspecialist in a timely manner.
Short-term outcomes after primary reverse total shoulder arthroplasty in patients with cervical spine pathology or previous cervical spine surgery compared to those without
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Citation Excerpt :
This study also demonstrated that patients with known c-spine pathology had worse postoperative patient-reported outcomes than patients without c-spine pathology, and did not demonstrate as significant improvement after rTSA. Evaluation of a patient who may benefit from rTSA should always include a careful examination of the c-spine, as c-spine pathology such as radiculopathy may mimic RTC dysfunction or be found in conjunction with RTC dysfunction [9,11]. The incidence of c-spine pathology in patients presenting with shoulder pain is thought to be considerably high.
Cervical spine (c-spine) and shoulder pathology have been known to cause similar symptoms and often co-exist, making an accurate diagnosis difficult, especially in an elderly population. Reverse total shoulder arthroplasty (rTSA) has been shown to decrease pain and improve quality of life when shoulder pathology is the source of pain and disability. The purpose of this study was to identify the prevalence of c-spine pathology in a cohort of patients who underwent rTSA and to compare postoperative outcome scores to a cohort without c-spine pathology.
A retrospective review was performed utilizing a single institution's operative records of primary rTSAs. Radiology reports, imaging, and operative reports were reviewed, and presence of any c-spine pathology or previous surgery were recorded. Additionally, postoperative outcome scores (American Shoulder and Elbow Surgeons [ASES], Constant Score, University of California, Los Angeles [UCLA], and Simple Shoulder Test [SST]) were evaluated at >2 years post-rTSA.
A total of 438 primary rTSA cases were evaluated. Of these, 143 (32.6%) had documentation of prior c-spine pathology and/or history of previous c-spine surgery. After applying further exclusion criteria, a total of 50 patients with c-spine pathology and 108 patients without c-spine pathology were found to have complete medical records and postoperative outcome scores to allow comparison between groups. Patients without c-spine pathology were found to have statistically higher postoperative UCLA, ASES, and SST scores when compared to patients with c-spine pathology. Patients without c-spine pathology also demonstrated a significant improvement in the difference between their postoperative and preoperative UCLA and ASES scores.
This study demonstrated a high prevalence of c-spine pathology (32.6%) in a cohort of patients who underwent primary rTSA. Additionally, short-term outcome scores of patients undergoing rTSA with concomitant c-spine pathology are significantly lower than those of patients without a history of c-spine pathology.
Effectiveness of Glenohumeral Joint Mobilization on Range of Motion and Pain in Patients With Rotator Cuff Disorders: A Systematic Review and Meta-Analysis
2023, Journal of Manipulative and Physiological Therapeutics
The purpose of this study was to determine the effectiveness of glenohumeral joint mobilization (JM) on range of motion and pain intensity in patients with rotator cuff (RC) disorders.
An electronic search was performed in the MEDLINE, CENTRAL, Embase, PEDro, LILACS, CINAHL, SPORTDiscus, and Web of Science databases. The eligibility criteria for selecting studies included randomized clinical trials that investigated the effect of glenohumeral JM techniques with or without other therapeutic interventions on range of motion, pain intensity, and shoulder function in patients older than 18 years with RC disorders. Two authors independently performed the search, study selection, and data extraction, and assessed risk of bias. Grades of Recommendation Assessment, Development and Evaluation ratings were used to evaluate the quality of evidence in this study.
Twenty-four trials met the eligibility criteria, and 15 studies were included in the quantitative synthesis. At 4 to 6 weeks, for glenohumeral JM with other manual therapy techniques vs other treatments, the mean difference (MD) for shoulder flexion was −3.42° (P = .006), abduction 1.54° (P = .76), external rotation 0.65° (P = .85), and Shoulder and Pain Disability Index score 5.19 points (P = .5), and standard MD for pain intensity was 0.16 (P = .5). At 4 to 5 weeks, for the addition of glenohumeral JM to an exercise program vs exercise program alone, the MD for the visual analog scale was 0.13 cm (P = .51) and the Shoulder and Pain Disability Index score was −4.04 points (P = .01).
Compared with other treatments or an exercise program alone, the addition of glenohumeral JM with or without other manual therapy techniques does not provide significant clinical benefit with respect to shoulder function, range of motion, or pain intensity in patients with RC disorders. The quality of evidence was very low to high according to Grades of Recommendation Assessment, Development and Evaluation ratings.
Efficacy of transdermal 4% lidocaine patches for postoperative pain management after arthroscopic rotator cuff repair: a prospective trial
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Postoperative pain management continues to be a challenging aspect of patient care. Lidocaine patches have shown efficacy in reducing pain in other surgical specialties and mixed results in orthopedic trials. We sought to determine the effectiveness of nonprescription lidocaine patches in reducing postoperative pain after arthroscopic rotator cuff repair
Patients undergoing primary arthroscopic rotator cuff repair were recruited from 3 surgeons at a single institution. All patients of each surgeon were randomized to a lidocaine patch or control group, with crossover occurring at the midpoint. Experimental group patients received 26 4% lidocaine gel-patches. They were provided written and visual instructions to begin wearing the lidocaine patches during daytime on postoperative day (POD) 2. They were to be switched every 8 hours and removed overnight. Control group patients received normal standard of care but did not receive a placebo control. Exclusion criteria included workmen’s compensation claims, age <18 years, history of myocardial infarction, and history of lidocaine or adhesive allergies. The American Shoulder and Elbow Surgeons shoulder survey was completed preoperatively and 2-, 6-weeks, 3-, 4.5-, and 6-months postoperatively. A 14-day visual analog scale pain and medication log was completed three times daily following repair. All patients received interscalene nerve block with bupivacaine and general anesthesia.
80 (40 control, 40 lidocaine) patients were enrolled, with 53 completing follow-up. Groups were demographically similar in age (P = .22), gender (P = .20), and body mass index (P = .77). They were similar in tear pattern (P = .95), concomitant acromioplasty (P = .44), concomitant biceps tenodesis (P = .07), and number of anchors used (P = .25). There was no difference in American Shoulder and Elbow Surgeons scores at any time points (range P = .28-P = .97). Reported 14-day pain logs were not different between study groups at any time points (range P = .07-P = .99). There was no difference in opioid consumption in the first 14 days after surgery (P = .38). The lidocaine group reported less satisfaction with their pain management beginning in the evening of POD 2 (P = .05). This continued until the afternoon of POD 8 (P = .03).
Transdermal 4% lidocaine patches are not effective in reducing pain or opioid consumption after arthroscopic rotator cuff repair and were associated with reduced patient satisfaction.
Association between type of rotator cuff tear and functional outcomes in patients with massive and irreparable rotator cuff tear: A pre-post intervention study
2021, Journal of Shoulder and Elbow Surgery
Citation Excerpt :
In addition, tobacco consumption degenerates the collagen quality that affects the tendon and shoulder function.4 Currently, it remains unclear whether the patients' symptoms or complaints are related to the type of tear, so the anatomic structure appears to be independent of functional outcomes and not necessarily associated with pain or symptom development.6,43,64 Some studies have shown an association between fatty infiltration and degenerative findings with shoulder function and a loss of range of motion in patients with a rotator cuff tear.41,55
The aim of this study was to analyze: (1) the differences in the pre-post change in functional outcomes after a physical therapy program by the type of massive and irreparable rotator cuff tear (MIRCT) controlling for potential confounders, and (2) the influence of lifestyle behaviors and demographic and tear tendon characteristics on function in patients over 60 years of age with conservatively treated MIRCT.
In this pre-post intervention study, 92 patients were prospectively recruited at the Clinical Hospital San Borja Arriaran, with atraumatic MIRCT, between 60 and 75 years of age (mean: 67.9 ± 4.5 years), and the mean of length of symptoms was 16.5 months (±5.7 months). Patients received a physical therapy program consisting of manual therapy and a specific exercise program of 2 sessions per week for 12 weeks. The imaging findings were performed by 2 medical radiologists who classified the rotator cuff tear according to the criteria proposed by Collins. Shoulder function, upper limb function, and pain intensity were assessed with the Constant-Murley; Disabilities of the Arm, Shoulder, and Hand; and visual analog scale (VAS), respectively. Analysis of covariance models were estimated to assess differences in MIRCT categories between functional outcomes. Multiple regression model analysis was used for the association between the change in functional outcomes and lifestyle behaviors, and demographic and tear tendon characteristics.
The results showed no pre-post change in functional outcomes by type of MIRCT in all models (P > .05). There is an association between length of symptoms (P = .000), and the baseline values of the 3 functional measures (P = .000) are associated with changes in Constant-Murley; Disabilities of the Arm, Shoulder, and Hand; and VAS. In addition, changes in VAS are associated with body mass index (BMI) (P = .000), and changes in Constant-Murley are associated with gender (P = .023), BMI (P = .000), and tobacco consumption (P = .000).
There is no difference in functional outcomes by type of MIRCT after a physical therapy program controlling for potential confounders. In addition, there is an association of length of symptoms with all functional outcomes, an association of BMI with VAS and Constant-Murley questionnaire, and an association between tobacco consumption and Constant-Murley questionnaire. Our results could influence the orthopedic surgeon's decisions; thus, not predicting the functional outcome through imaging findings could lead clinicians to reconsider the need for surgery in the treatment algorithm in patients over 60 years with MIRCT. In addition, demographic characteristics and lifestyle behaviors might be considered within the patient's evaluation and follow-up to decide on surgical interventions and evaluate the clinical course of the disease. Further studies measuring additional variables and longer follow-up are needed to confirm these results.

View all citing articles on Scopus

: Funding: The source of funding for this study was NIH R01 HD073180.

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Review ArticleThe role of the peripheral and central nervous systems in rotator cuff disease

Section snippets

Proprioceptors and related spinal reflexes

Central processing of proprioceptive information

Nociceptors and peripheral and central pain processing

Motor nerves and neuromuscular junction

Sensory nerves

Shoulder muscle activity and kinematics

Motor cortical changes

Conclusion and perspective

Disclaimer

J Shoulder Elbow Surg

Ann Anat

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

Arthroscopy

J Shoulder Elbow Surg

J Electromyogr Kinesiol

J Shoulder Elbow Surg

Br J Anaesth

Arthroscopy

Eur J Pain

J Shoulder Elbow Surg

Neuroscience

J Shoulder Elbow Surg

Brain Stimul

Exp Neurol

Pain

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

Arthroscopy

Exp Neurol

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

J Shoulder Elbow Surg

Exp Neurol

Innervation of the human shoulder joint and its implications for surgery

Clin Orthop Relat Res

Force steadiness, muscle activity, and maximal muscle strength in subjects with subacromial impingement syndrome

Muscle Nerve

Motor consequences of experimentally induced limb pain: a systematic review

Eur J Pain

Dynamic upper limb proprioception in multidirectional shoulder instability

Clin Orthop Relat Res

Variations in anatomy at the suprascapular notch possibly causing suprascapular nerve entrapment: an anatomical study

Knee Surg Sports Traumatol Arthrosc

Pain inhibition of shoulder strength in patients with impingement syndrome

Orthopedics

Long-term effects of tenotomy on spinal monosynaptic response in the cat

Science

Central neuromuscular dysfunction of the deltoid muscle in patients with chronic rotator cuff tears

J Orthop Trauma

Suprascapular neuropathy

J Bone Joint Surg Am

The biology and restorative capacity of long-term denervated skeletal muscle

Basic Appl Myol

Surgical options for patients with shoulder pain

Nat Rev Rheumatol

Subacromial injection improves deltoid firing in subjects with large rotator cuff tears

HSS J

Human evolution and tears of the rotator cuff

Int Orthop

Suprascapular nerve entrapment

J Bone Joint Surg Am

Overuse of training increases mechanoreceptors in supraspinatus tendon of rats SHR

J Orthop Res

The peripheral neuronal phenotype is important in the pathogenesis of painful human tendinopathy: a systematic review

Clin Orthop Relat Res

Why does my shoulder hurt? A review of the neuroanatomical and biochemical basis of shoulder pain

Br J Sports Med

Repair of ruptures of the rotator cuff of the shoulder

Br J Sports Med

Fatty degeneration and atrophy of the rotator cuff muscles after arthroscopic repair: does it improve, halt or deteriorate?

Arch Orthop Trauma Surg

Review Article
The role of the peripheral and central nervous systems in rotator cuff disease