https://orcid.org/0009-0000-7986-7931
ABSTRACT
Introduction
A significant number of rotator cuff tear (RCT) patients developed chronic shoulder pain that did not correspond to physiological changes. Central sensitization syndrome (CSS) is a neurophysiological adaptation process that can result in hypersensitivity to peripheral stimuli. Although there is evidence of an association between CSS and musculoskeletal problems, no studies have focused on the association between CSS and RCT. The primary purpose of this study was to examine the prevalence of CSS in patients with RCT. The secondary purpose was to document the associated conditions and comorbidity that were associated with the CSS.
Methods
This was a cross-sectional study of patients with RCT who completed the Central Sensitization Inventory (CSI). Patients with score of ≥ 40/100 were considered positive for CSS. Demographic and clinical data and CSI results were collected to analyze the prevalence and associated factors of CSS in RCT patients.
Results
A total of 404 RCT patients were included, and the CSS prevalence was 39.4%. Compared to the non-CSS group, the CSS group had an odds ratio of 4.13 (95% CI, 2.70–6.32; p＜0.001) for ages 51–60, 3.07 (95% CI, 2.00–4.69; p＜0.001) for symptoms lasting more than 6 months, 6.08 (95% CI, 3.90–9.47; p＜0.001) for nonphysical laborers, 3.69 (95%CI, 2.42–5.61; p＜0.001) for long head of biceps (LHB) abnormality, 2.93 (95% CI, 1.93–4.45; p＜0.001) for concurrent shoulder stiffness, 4.82 (95% CI, 2.55–9.10; p＜0.001) for anxiety or panic episodes, and 2.11 (95% CI, 1.12, 4.00; p＜0.001) for depression.
Conclusions
The prevalence of CSS in patients with RCT was relatively high at 39.4%. The CSS was associated with higher age, female gender, and clinical findings of symptoms lasting over six months, nonphysical laborers, abnormal LHB, concurrent shoulder stiffness, anxiety, and depression.
Introduction
Persistent shoulder pain in patients with rotator cuff tear (RCT) is a great problem, leading to increased opioid use, delayed recovery, and heavy economic burdens [Citation1]. Previously, physiological factors such as age, fatty infiltration, tear size, and metabolic diseases got more attention [Citation2]. However, the pain feelings do not usually correlate with the severity of physiological alterations even a successful rotator cuff repair surgery has been performed [Citation3]. Recently, increasing emphasis has been placed on psychologic factors and sensory neuroplasticity, as accumulating studies have found that they are closely associated with chronic musculoskeletal pain [Citation4–8], especially shoulder pain [Citation9–14].
As a plausible explanation for persistent shoulder pain, altered somatosensory perceptions and sensitization of the central nerve systems have been proposed [Citation9,Citation15,Citation16]. Central sensitization Syndrome (CSS) is an adaptive, activity-dependent, and dynamic neurophysiological process characterized by increased excitability, more intense synaptic transmission, and decreased inhibition of dorsal horn neurons [Citation4]. In the short term, CSS can be beneficial and protective, but in the long run, it can be maladaptive and lead to chronic pain, even disability.
Historically, different terms have been used to describe CSS symptoms, such as ‘functional somatic syndromes,’ ‘medically unexplained symptoms,’ and ‘bodily distress syndrome.’ These syndromes share various characteristics, including chronic pain, fatigue, poor sleep, cognitive impairments, headaches, anxiety, and depression. These self-report comorbidities consist of part of the Central Sensitization Inventory (CSI), which will be described in the ‘Outcome Measures’ section. A significant percentage of RCT patients suffer from these symptoms for a long time, even after surgery [Citation12]. Until the development of the CSI, the evaluation and diagnosis of CSS remain difficult [Citation17]. The CSI has been shown to have good clinical validity and reliability in detecting CSS [Citation18], but no study has used it in the assessment of patients with RCT.
Given the close relationship between CSS and significant symptoms of patients with RCT, there is a need to investigate the prevalence of CSS in the RCT population. The primary purpose of this study was to examine the prevalence of CSS in patients with RCT. The secondary purpose was to document the associated conditions and comorbidity that were associated with the CSS.
Methods
Compliance with ethics guidelines
This was a single-center cross-sectional study. The study was approved by the Ethics Committee of West China Hospital (2020934), and was performed in accordance with the Declaration of Helsinki. All patients provided informed consent prior to data collection.
Study Participants
Consecutive patients referred to an academic clinic center from 15 January 2022 to 30 April 2023, with a confirmed diagnosis of partial or full-thickness RCT were approached to participate in the study.
The inclusion criteria were as follows: (1) confirmed magnetic resonance imaging (MRI) evidence of unilateral full-thickness RCT or Ellman grade III partial-thickness RCT [Citation19]; (2) over 18 years old; (3) and completed CSI. The exclusion criteria were as follows: (1) other disorder (Outerbridge IV or V osteoarthritis, infection, labral tear or instability which needs surgery) of the affected shoulder; (2) history of previous surgical procedures in the affected shoulder; (3) history of previous head or spine injury; (4) central nervous system diseases or diseases that could negatively impact the central nervous system; (5) undergoing psychological medical treatment or using narcotic medication regularly; (6) or refusal to participate.
Demographic information
Two independent researchers assisted patients to complete the CSI and collected demographic and clinical data from medical histories and interviews for each enrolled patient. Disagreements were solved by a third researcher.
Demographic data included age (subgroups were 18–40; 41–50; 51–60; 61–70; ＞70), sex, affected shoulder, body mass index (BMI) (subgroups were＜18.5; 18.5–24.9; 25.1–29.9;＞30) [Citation20],
Clinical data included duration of symptoms (subgroups were ≤6 months;＞6 months), occupation (subgroups were physical laborers and nonphysical laborers), smoke status (subgroups were smoker and nonsmoker), rotator cuff tear size (subgroups were ＜1 cm, 1-3 cm, 3-5 cm,＞5 cm), subscapularis type (subgroups were complete and torn), long head of biceps (LHB) type (subgroups were normal and abnormal), and concomitant shoulder stiffness (the shoulder stiffness was defined as a loss of at least half of active and passive shoulder range of motion [Citation21,Citation22], and subgroups were stiff and non-stiff). These clinical data were included because they are related to the mental health and CSS according to previous studies [Citation12,Citation14,Citation23].
Outcome measures
The CSI is consisted of two parts: part A included 25 questions about presence and intensity of CSS-related symptoms using a 0–4 Likert scale (0, never; 1, rarely; 2, sometimes; 3, often; 4, always); and part B investigated if there was any previous diagnosis of central sensitivity syndromes (CSSs), which includes restless leg syndrome, chronic fatigue syndrome, fibromyalgia, temporomandibular joint disorder, migraine or tension headaches, irritable bowel syndrome (IBS), multiple chemical sensitivities, neck injury, anxiety or panic attacks, and depression [Citation17]. As a CSI part A score ≥ 40 has been proved effective to identity patients with CSS [Citation18], all enrolled patients were divided into CSS group (CSI part A score ≥ 40) and non-CSS group (CSI part A score＜40). Previous studies have proven that CSI has good validity in musculoskeletal disorders [Citation17,Citation18,Citation24–27].
Statistical analysis
All categorical data were presented as numbers and percentages, whilst numerical variables were summarized as means and standard deviations. The significance level was set at 0.05. All analyses were performed with SPSS, version 22.0 (SPSS Inc., Chicago, IL, U.S.A.). The chi-square test, Fisher’s exact test, or t test were used to assess differences in demographic and clinical variables between patients with and without CSS. For multiple comparisons of proportions between subgroups, the Bonferroni method was used. The variables with a significant association with CSS were then included in a multivariable logistic regression model and selected further using a backward stepwise approach.
PASS software version 15.0 (NCSS, LLC, Kaysville, Utah, U.S.A.) was used to conduct a power analysis. We found that at least 267 patients would have ensured a precision of ±6% for a 95% 2-sided CI formed around this point estimate, assuming a CSS prevalence of 50%, which resulted in the maximization of variance and sample size [Citation28].
Results
During the study period, 476 consecutive patients with RCT were invited to this study. Seventy-two patients (15.3%) met the exclusion criteria and were eliminated: 42 patients (58.3%) were Ellman grade I or II partial-thickness RCT, 5 patients (11.9%) were with labral tear or shoulder instability, 12 patients (16.7%) had previous surgical treatments on the affected shoulder, 8 patients (11.1%) had neurologic diseases, and 5 patients (13.6%) refused to participate. Finally, data of 404 patients were used for analysis ().
Figure 1. Patient selection flowchart.
The mean age of the 404 enrolled patients was 58.22 ± 12.76, and the mean BMI was 23.43 ± 4.96. Most patients were 51–60 years old (40.10%), female (60.14%), right shoulder affected (56.93%), BMI ranged 18.5–24.9 (45.54%), symptoms lasted more than 6 months (54.95%), physical laborers (51.98%), nonsmokers (59.16%), 1-3 cm tear size (49.00%), complete subscapularis, normal LHB (57.92%), and non-stiff shoulders (61.88%). demonstrates the demographic and clinical characteristics of the study population.
Table 1. Clinical characteristics of the study population.
Prevalence of CSS
A total of 159 patients were diagnosed with CSS (CSI part A score 40), resulting in a 39.4% (159/404) prevalence of CSS among these consecutive patients. The detailed CSI results were shown in .
Table 2. Central Sensitization Inventory (CSI) results.
Demographics, clinical, and self-report comorbidity
No significant difference between patients with CSS and without CSS in terms of affected shoulder, BMI, smoke status, rotator cuff tear size, and subscapularis type was found. However, in terms of age, gender, duration of symptoms, occupation, LHB type, and shoulder stiffness, there were significant differences in proportion distribution between the CSS and non-CSS groups (). As for CSI part B outcomes, only the incidences of anxiety or panic attacks and depression were significantly higher in the CSS group ().
Table 3. Clinical characteristics comparisons between the CSS group and the non-CSS group.
Table 4. CSI part B comparisons between the CSS group and the non-CSS group.
According to multivariable logistic regression, when compared to the non-CSS group, patients in the CSS group had an odds ratio of 4.13 (95% CI, 2.70–6.32; p＜0.001) for ages 51–60, 3.07 (95% CI, 2.00–4.69; p＜0.001) for symptoms lasting more than 6 months, 6.08 (95% CI, 3.90–9.47; p＜0.001) for nonphysical laborers, 3.69 (95%CI, 2.42–5.61; p＜0.001) for long head of biceps (LHB) abnormality, 2.93 (95% CI, 1.93–4.45; p＜0.001) for concurrent shoulder stiffness, 4.82 (95% CI, 2.55–9.10; p＜0.001) for anxiety or panic episodes, and 2.11 (95% CI, 1.12–4.00; p＜0.001) for depression ().
Table 5. Multivariable logistic regression analysis for CSS (yes/no).
Discussion
The primary finding of this study was that the prevalence of CSS among patients with RCT is approximately 39.4%, which is higher than previously reported prevalence in other musculoskeletal disorders (37.8% in low back pain, 32.4% in neck pain, 13.5% in upper back pain, and 8.1% in knee pain) [Citation29]. In addition, female patients aged 51–60 years old, symptoms lasting over 6 months, nonphysical laborers, concurrent shoulder stiffness, anxiety of panic attacks, and depression were associated factors for RCT patients with CSS.
Even after a successful arthroscopic rotator cuff repair, a considerable proportion of RCT patients experience persistent chronic shoulder pain that is accorded to physiological changes. The underlying mechanisms of obstinate shoulder pain remain controversial. Recently, CSS has been considered to be one of the most important reasons of chronic pain [Citation9–14]. Hypersensitivity to peripheral stimuli, neuropathic pain, and referred pain, which were considered to be peripheral manifestations of CSS, have been widely observed in fibromyalgia, osteoarthritis, musculoskeletal disorder, neuropathic pain, headache, visceral pain hypersensitivity disorders, dental pain, temporomandibular joint disorders, and postsurgical pain in clinical cohort studies [Citation30].
Previous researches merely discovered an association between CSS and rotator cuff tendinopathies. Gwilym et al. (2011) [Citation10] studied 17 patients with unilateral shoulder impingement syndrome and 17 age- and gender-matched controls in 2011. They confirmed the presence of CSS in patients with shoulder impingement syndrome, and preoperative CSS is associated with poorer 3-month surgical results following subacromial decompression. Similarly, King et al. (2022) [Citation31] compared unilateral shoulder impingement syndrome patients to controls. They found the presence of peripheral sensitization for all patients, and both peripheral and CSS for female patients. Plinsinga et al. (2015) [Citation8] performed a systematic review to determine whether CSS exists in those who have persistent rotator cuff, lateral elbow, and patellar tendinopathies. With 16 studies (4 shoulder impingement syndrome, 10 lateral epicondyle tendinopathy, and 2 patellar tendinopathy) included, they concluded that there is an association between persistent tendon pain and CSS. Another systematic review by Noten et al. (2017) [Citation13] also concluded that musculoskeletal shoulder pain might be closely connected with the central nervous system. A recent cross-sectional study focused on the prevalence of CSS in people with chronic musculoskeletal pain problems [Citation29]. They found CSS in 37.8% of patients with low back pain, 32.4% with neck pain, 13.5% with upper back pain, 8.1% with knee pain, and 2.1% with shoulder pain. However, they only included 22 shoulder pain patients without a confirmed diagnosis. Therefore, research on the relationship between CSS and RCT is still absent.
To the best of our knowledge, this study was the first to investigate the prevalence of CSS in patients with RCT. We did not only find that the prevalence of CSS among patients with RCT is approximately 39.4%, but also identified associated factors for RCT patients with CSS.
In the included RCT patients, female patients were considerably more likely to develop CSS than male ones. The CSS group had 82.39% (131/159) female patients, while the non-CSS group had only 45.71% (112/245) female patients. This sex-specific characteristic is in line with the study by King et al. (2022) [Citation31], in which CSS was only evident in female patients, but peripheral sensitization was observed in all individuals. Previous research has found that female patients with rotator cuff disease have a higher risk of repetitive injuries and disability, increased drug usage, and a longer duration from injury to surgery [Citation32,Citation33]. Epidemiologic and clinical studies clearly showed that women are more likely than men to suffer from chronic pain, and some evidence suggested that women may experience more severe pain. Experimentally induced pain studies have yielded very similar results, with women demonstrating greater susceptibility to develop severe pain and CSS as compared to men [Citation34]. Our study confirmed that female RCT patients are at a higher risk of developing CSS than male patients.
For these RCT patients, age is another risk factor. The CSS group had 60.38% patients aged 51–60 and 22.01% patients aged 61–70, while the non-CSS group only had 26.94% and 24.49%, respectively. RCT is an age-related disease, with the incidence of full-thickness RCT rising from 6% in the population under 60 to 30% in those over 60, and over 50% in those over 80 [Citation35]. Furthermore, earlier studies have indicated that older patients, particularly older women, have a higher prevalence of chronic pain than younger groups of patients [Citation36,Citation37]. Our study revealed that the predominant group of patients diagnosed with CSS were women between the ages of 51 and 60. This observation may be attributed to the higher likelihood of this particular subgroup undergoing surgical procedures, and our center primarily focuses on treating surgical patients. However, there was no significant relationship between CSS and BMI, affected shoulder, or smoking status.
Symptoms that lasted more than 6 months, abnormal LHB, and shoulder stiffness were all risk variables closely associated with the RCT. In the CSS group, 71.07% of patients had symptoms for more than 6 months, 61.01% had abnormal LHB, and 53.46% had shoulder stiffness, whereas the non-CSS group only had 44.49%, 29.80%, and 28.16%, respectively. These findings were consistent with earlier research, which showed that long-lasting symptoms, LHB pathology, and shoulder stiffness were all associated with poor postoperative outcomes [Citation38–42]. LHB pathology often coexists with rotator cuff degeneration, causing further inflammatory changes in the LHB tendon, which can be quite painful and debilitating. The mechanism is currently unknown, although four major possibilities have been proposed. The mechanical theory suggests that repetitive loading leads to microscopic degeneration, activating fibroplasia and resulting in scar tissue formation. The vascular theory explains tendon degeneration with focal vascular disruption. The apoptosis theory points to increased programmed cell death causing tissue degeneration. Lastly, the neural theory proposes that neurally-mediated mechanisms, like mast cell degranulation, substance P and alarmins release, contribute to LHB-related neuropathic pain [Citation38]. Similarly, shoulder stiffness is frequently associated with microscopic degeneration, fibroplasia activation, angiogenesis, scar tissue development, and the production of neuronal mediators such as alarmins, all of which can lead to persistent neuropathic pain [Citation21,Citation22,Citation43,Citation44]. However, neither rotator cuff tear size nor subscapularis type were observed to have a significant relationship with CSS. A previous cross-section study by Dunn et al. (2014) has proven that symptoms of pain do not correlate with rotator cuff tear severity [Citation3]. Although the etiology of subscapularis lesions is still largely unclear, a recent research found a strong correlation between subscapularis lesions and the morphology of the coracoid process and the humeral version [Citation45]. The fact that mechanical mechanisms, not neural mediators, were the main causes of subscapularis lesions, may help to explain why subscapularis lesions are not related factors of CSS.
In this study, occupation were identified as two significant associated factors for RCT patients with CSS. In the CSS group, 73.58% of patients were nonphysical laborers, 23.90% had anxiety or panic attacks, and 15.09% were depressed, compared to 31.43%, 6.12%, and 7.76% in the non-CSS group, respectively. The connection between occupation and CSS in RCT patients revealed in this investigation differed from earlier studies, which found that non-manual workers were less likely than manual workers to suffer chronic pain [Citation46]. A possible explanation would be that physical laborers in this area experienced much more musculoskeletal disorders at younger ages, and thus had a higher tolerance to pain at older ages when the rotator cuff disease developed. Further research into the relationship between occupation and CSS in RCT patients is needed.
As for mental health, accumulating evidence have proved that mental health has a strong relationship with poor postoperative self-assessed functions and pain for RCT patients [Citation47–51]. Our research found that RCT patients who had anxiety or panic attacks, as well as depression, were at a considerably increased risk of acquiring CSS. To ascertain if modifications in central pain processing affect prognosis following rotator cuff repair, a prospective longitudinal cohort research [Citation52] has been designed, and the forthcoming findings are noteworthy.
Given a relatively high prevalence of CSS in patients with RCT, recognizing patients with CSS is crucial, so the CSI could be considered a standard assessment for patients with RCT, especially for those with associated factors. Then, individuals with CSS might benefit from enhanced pain management, psychological counseling, and customized rehabilitation. Implementing these strategies could be helpful in optimizing patient outcomes and satisfaction.
Limitations
There were some limitations of this study. First, as our study is cross-sectional in nature, it does not allow for the assessment of disease progression within individual patients over time, consideration of generational differences, or the establishment of causal relationships. This limitation restricts our ability to draw conclusions regarding the temporal aspects and causality of central sensitization in patients with RCT. However, we acknowledge that cross-sectional studies are valuable in estimating prevalence and identifying associated factors. We have taken this into account when interpreting our findings. Second, because the CSI is a self-assessment questionnaire, patients may have a significant impact on the results. In order to evaluate the CSS, additional research needs gather objective criteria such sensory hypersensitivity determined by quantitative sensory testing. Third, given that our center is a surgical department and that the majority of the patients enrolled were candidates for surgical procedures, the severity of RCT might be higher. Those who do not require surgical treatments should be the focus of future research.
Conclusions
The prevalence of CSS in patients with RCT was relatively high at 39.4%. The CSS was associated with higher age, female gender, and clinical findings of symptoms lasting over six months, nonphysical laborers, abnormal LHB, concurrent shoulder stiffness, anxiety, and depression.
Declaration of financial/other relationships
The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties. Peer reviewers on this manuscript have no relevant financial or other relationships to disclose.
Author contributions
Investigation, data analysis, writing – original draft preparation: Run Peng. Writing – review & editing, supervision: Ning Ning. Writing – review & editing, conceptualization: Rong Yang.
Additional information
Funding
References
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