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 Table of Contents  
Year : 2019  |  Volume : 13  |  Issue : 2  |  Page : 102-108

Recognition of central nervous system sensitization and its risk factors in patients with unilateral musculoskeletal shoulder pain

1 Department of Physiotherapy, Sarvajanik College of Physiotherapy, Surat, Gujarat, India
2 Senior Physiotherapist, SJ Nursing Home, Nagercoil, Tamil Nadu, India

Date of Submission15-May-2018
Date of Decision10-May-2019
Date of Acceptance03-Jun-2019
Date of Web Publication07-Oct-2019

Correspondence Address:
Dr. Thangamani Ramalingam Alagappan
Sarvajanik College of Physiotherapy, Surat - 395 003, Gujarat
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/PJIAP.PJIAP_17_18

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BACKGROUND: Overall, inferences from the majority of the literatures reviewed provide increasing evidence on the presence of central nervous system sensitization in unilateral shoulder pain. The possibility of presence of central sensitization (CS) among patients with unilateral musculoskeletal shoulder pain has not been adequately explored till date. The term “unilateral shoulder pain” in this study will be used to refer to nonneuropathic shoulder pain of different etiologies including rotator cuff pathology, adhesive capsulitis, or labral lesion.
OBJECTIVES: The purpose of this study was to determine the presence of a subgroup of patients among patients with unilateral musculoskeletal shoulder pain and to further explore what extent the central nervous system sensitization correlates with other clinical measures.
METHODS: Ninety-one patients with unilateral musculoskeletal shoulder pain participated in this cross-sectional study. Standardized outcome measures such as Central Sensitization Inventory-Gujarati (CSI-G) for the presence of CS, pressure pain threshold by pressure algometry, and Shoulder Pain and Disability Index for disability were administered as per standardized protocol.
RESULTS: The results of the present study showed that 17 (18.7%) patients had CS. The CSI score had mild correlation with the demographic and clinical outcome measures and comorbidities such as gender (r = 0.208), duration of the condition (r = 0.208), hypertension (r = −0.238), sleep disturbance (r = −0.327), numbness (r = −0.238), and fatigue perception (r = −0.314) by the pain and disability score also had mild correlation with CSI score (P, 0.05). The risk ratio for sensitization was 2.40 for female gender, 3.07 for hypertension, 3.19 for sleep disturbance, 2.06 for numbness, and 3.87 for perceived fatigue in patients with unilateral musculoskeletal shoulder pain.
CONCLUSION: The present study showed that the central nervous system becomes hypersensitive in a subgroup of patients and weakly related to factors such as female gender, chronicity of shoulder pain, hypertension, pain and disability, sleep disturbance, and perceived fatigue in patients with unilateral musculoskeletal shoulder pain.

Keywords: Central sensitization, disability, pressure pain threshold, shoulder pain, unilateral musculoskeletal shoulder pain

How to cite this article:
Alagappan TR, Senthilkumar S N, Dhanani DP, Vashi RH, Barot DN, Savani MN. Recognition of central nervous system sensitization and its risk factors in patients with unilateral musculoskeletal shoulder pain. Physiother - J Indian Assoc Physiother 2019;13:102-8

How to cite this URL:
Alagappan TR, Senthilkumar S N, Dhanani DP, Vashi RH, Barot DN, Savani MN. Recognition of central nervous system sensitization and its risk factors in patients with unilateral musculoskeletal shoulder pain. Physiother - J Indian Assoc Physiother [serial online] 2019 [cited 2022 Oct 7];13:102-8. Available from: https://www.pjiap.org/text.asp?2019/13/2/102/268638

  Introduction Top

Shoulder pain is the third-most common musculoskeletal disorder in the general population, with point prevalence rates ranging from 6.9% to 26% and lifetime prevalence up to 66.7%.[1] Common structural pathologies contributing to unilateral musculoskeletal pain in the reported literature but with varying degrees are the tear of the fibrocartilaginous labrum of the anterior half of the rim of the glenoid cavity along with capsule, periosteal tear of the anterior surface of the neck of the scapula (Bankart's lesion), impingement syndrome or rotator cuff tendinitis due to compression of the cuff in the subacromial arch, frozen shoulder, or adhesive capsulitis.[2],[3],[4]

Currently, the treatment for symptoms of musculoskeletal shoulder pathology such as pain, impaired work, and leisure activities due to difficulty in overhead movements are predominantly symptomatic. Due to limited understanding of the pain symptoms in the above-mentioned shoulder pathologies, it is postulated that, in the injury healing process, the pathological changes as a result of inflammation and related physiological processes may provoke the development of peripheral sensitization, central sensitization (CS), and neural plasticity.[2] This sensitization issue leads to increase in nociception when the innocuous input is sensed as pain. CS is considered an amplification of signaling (pain hypersensitivity) encloses, malfunctioning of descending pain inhibitory mechanisms, enhanced activity of pain facilitatory mechanism, and long-term potentiation of the neural synapses in the anterior cingulated cortex within the central nervous system.[3],[4] This could be a prolonged distorted sensory processing in the central nervous system, but reversible increase in the excitability, may be homosynaptic or heterosynaptic, spinal segmental or nonsegmental which is dependent or independent of continuous peripheral input from unimodal and polymodal receptors leading to generalized or widespread hypersensitivity.[4],[5],[6] Usually, the characteristics of CS are allodynia (painful sensation to a normally nonpainful stimulus such as touch), hyperalgesia (excessive sensitivity to a normally painful stimulus such as pressure), expansion of receptive field (pain that extends beyond the area of peripheral nerve supply), and prolonged pain after the stimulus has been removed (usually, burning, throbbing, tingling, or numbness). The deregulation in both ascending and descending central nervous system and chronic release of pro-inflammatory cytokines by the immune system as a result of physical trauma or viral infections may lead to the development of CS. The label “central sensitivity syndrome (CSS)” has been preferred to describe syndromes for which no specific organic cause can be found related to CS such as fibromyalgia, chronic fatigue, irritable bowel syndrome, and temporomandibular disorder. The usual features of the above-mentioned syndromes are pain, fatigue, poor sleep, cognitive deficits, headache, anxiety, and depression. These features indicate the common etiology of Central Sensitization Rk II.[7] Hence, in this study, we postulated the assumption that similar increased excitability or CS of the central nervous system could be a cause associated with pain experienced by patients with unilateral chronic shoulder pain also. On the basis of literature review, CS is associated with chronic pain conditions such as whiplash, chronic fatigue syndrome, and also with unilateral shoulder pain such as rotator cuff tendinopathy, sub-acromial impingement syndrome, and frozen shoulder.[8],[9],[10]

Hence, the main objectives of the present study were to find out whether a subgroup of unilateral shoulder pain patients with the presence of central nervous system sensitization exists and to what extent does it correlate with other clinical measures mentioned in the review above. Hence, we aimed to measure central nervous system sensitization through both subjective and objective measures to achieve a clear understanding of the phenomenon in unilateral shoulder pain patients. Moreover, the association of central nervous system sensitization to clinical measures such as pain, disability, and somatization behavior was also assessed.

  Methods Top

Patient recruitment

This cross sectional study recruited patients with unilateral shoulder pain f hospitals and physiotherapy clinics in the geographical area where the study conducted. The patients were included in the study after satisfying the inclusion and exclusion criteria. Informed consent was taken from all the patients before participation. Exclusion criteria were patients with pain of cervical spine origin, neuropathic pain, and bilateral musculoskeletal shoulder pain. Inclusion criteria were patients with frozen shoulder, ligament tears, muscular pain, fractures, Bankart's lesion, impingement syndrome, postsurgical conditions, dislocation of shoulder, instability, tendinitis, tendon rupture, and arthritis.

Tools and procedure

Pressure pain threshold-pressure algometry

Pressure pain threshold (PPT) is an estimate of mechanical pain sensitivity. A handheld algometer which is a standardized instrument was used to measure PPT.[11] The patients were asked to lie down in supine position. After attaining this position, the readings of ipsilateral and contralateral tibialis anterior muscle were taken by the handheld algometer. Later, the patients were asked to change the position from supine to side lying position. Readings on both contralateral (unaffected) and ipsilateral shoulders were taken. The patients have to report when the feeling of pressure alone changes into a feeling of pressure and pain (pain detection threshold). Two readings were taken which had a time interval of 30 s, and the mean of two readings was taken. A lower PPT is indicative of decreased nociceptive thresholds to pain and signifies the presence of sensitization. The identification of lower PPT at tissues remote to the affected shoulder supports the presence of CS in those with unilateral shoulder pain.[3]

Central Sensitization Inventory

The Central Sensitization Inventory (CSI) is a standardized screening instrument (self-reported) which is being used to help better assess the symptoms thought to be associated with CS in order to aid physicians and other clinicians in syndrome categorization, sensitivity, severity, identification, and treatment planning, and to help minimize, or possibly avoid, unnecessary diagnostics and treatment procedures. The CSI part A consists of 25 statements related to the current health symptoms. Each of these items is measured on a 5-point temporal Likert's scale: never (0), rarely (1), sometimes (2), often (3), and always (4). A cumulative score ranges from 0 to 100. In addition, information is collected in part B on previously diagnosed CSS and related conditions.[7] This scale which is used is reliable and valid.[12] Scores ≥40/100 indicate the presence of CS. The CSI has good clinometric properties for assessing symptoms of CS in patients with chronic pain. The results of this questionnaire were used to divide the sample into two subgroups; one containing persons with a clinically relevant degree of symptoms of CS (CSI score ≥40) and the other containing persons with a lower degree of these symptoms (CSI score <40).[13],[14]

Shoulder Pain and Disability Index

The Shoulder Pain and Disability Index (SPADI) (self-reported) contains 13 items that assess two domains, a 5-item subscale that measures pain, and an 8-item subscale that measures disability. In the Numerical Rating Scale SPADI, there is a 0–10 scale, and the patient is asked to circle the number that best describes the pain or disability. Each subscale is summed and transformed to a score out of 100, with higher score indicating greater impairment or disability.[15]

Goniometry and manual muscle testing

Standardized goniometry tool and manual muscle testing using the Medical Research Council's grading were used to assess shoulder range of motion and strength of muscles as per protocol.[16],[17]

Statistical analysis

Data collected were cleaned for paucity and checked for normality with Kolmogorov–Smirnov test before the analysis, and categorical variables were presented in percentages and numerical variables in terms of mean and standard deviations for the demographic and clinical outcomes. Based on the CSI score, patients were categorized as no CS, subclinical CS, mild-moderate CS, and severe CS. A Pearson's moment correlation coefficient analysis between the objective and subjective measures of CS and other variables was done. The outcome measures were compared by an independent t-test to find the difference between no CS and CS-present group. A risk ratio calculation using cross tab was done for categorical outcomes. A structural equation modeling (SEM) was done using IBM SPSS AMOS software to confirm the factors and its association with CS in unilateral shoulder pain. All the analyses were done using IBM SPSS statistics for Windows, version 20.0 (IBM Corp, Armonk, NY, USA). Statistical significance was set at “P < 0.05” for all statistical analyses.

  Results Top

The present study collected data from 91 patients with unilateral shoulder pain with a mean age of 53.17 ± 13.56 years. The patients were matched for gender, with 49 (53.8%) males and 42 (46.2%) females in the selected sample. The personal, demographical, and clinical data of the patients are summarized in [Table 1] and [Table 2]. [Figure 1] shows the classification of CS distribution among patients in the study for recognition of central nervous system sensitization and its risk factors in unilateral musculoskeletal shoulder pain patients. [Table 3] and [Table 4] summarize the correlation of CSI score with the clinical and demographic variables and its risk ratio calculation to represent CS. [Table 5] summarizes the mean difference of CS and no CS groups for the outcome measures. The SEM results with observed variables such as CSI score as endogenous and duration of condition, hypertension, sleep, numbness, fatigue, and SPADI total pain as exogenous are shown in [Table 6] and [Table 7]; [Figure 2].
Table 1: Personal demographical data of the patients

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Table 2: Clinical outcome data of the patients (n=91)

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Table 3: Correlation analysis between CS score and the other outcome measures

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Table 4: Risk ratio of factors associated with central nervous system sensitization

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Figure 1: Classification of central sensitization

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Table 5: Comparison of no central sensitization/central sensitization-present group for outcome measures

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Table 6: Regression weights of the structural modeling analysis

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Table 7: Model fit indices for structural equation modeling model

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Figure 2: Structural equation modeling

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  Discussion Top

This study was aimed at identifying whether the subgroup of patients that exists in a selected sample of patients suffering from unilateral shoulder pain showed the effects of CS in the study. In the selected sample, 27 out of the 91 patients had the duration of the condition more than 6 months, which is the time for chronicity to develop as reported in the existing literatures and when adaption in pain mechanism for symptoms akin to CS could develop.[18] Comparison statistics also reflected statistical significance (P < 0.005) for duration of the condition (>6 months) for the presence of CS in our selected sample, supporting that, the higher the duration of a shoulder problem, the more likely is a chance of developing central sensitivity to pain [Table 5]. The cause of shoulder pain was near to even distribution in the selected population, and thus could not associate to the CS for any specific mechanism of the injury. The systemic factors such as diabetes and hypertension were evenly matched in the study sample for patients with CS, where the above-mentioned two factors could be a contributing factor for chronicity of any injury and here the shoulder injury. The study used translated version of CSI as one of the core tools in this study to identify cross-cultural adaptation of a validated tool to explore the presence of CS and its relation with clinical measures. A previous study reported positive result of using this inventory as a valid tool for screening as well as outcome measure, but the CSI was evaluated on low back pain patients.[19] Our previous study on cross-cultural adaptation of this tool showed encouraging result of this to be used as a valid clinical instrument. The result of the present study showed that, of the total sample, 17 (18.7%) patients had CS score of > 40 in CSI assessment tool, indicating that there exists a subgroup of patients with CS in unilateral musculoskeletal shoulder pain in a cross-cultural setting [Table 1]. However, one previous review on CS in shoulder pain reported of a need for further understanding of central pain sensitization and did not report of proportion of the subgroup of patients.[20] Another study reported that the severity or intensity of pain in CS is primarily dependent on pain catastrophizing psychological variable.[21] Neblett et al. described five categories of CSI severity ranging from subclinical (0–29), mild (30–39), moderate (40–49), severe (50–59), and extreme (60–100) based on CSI scores [Table 1] and [Figure 1].[12]{Table 1}

The presence of a subgroup of sensitized patients with unilateral shoulder pain is supported by the present study, which is similar to other previous studies done on this topic.[4],[5] The chronicity of condition in patients clearly impacts the transition from peripheral sensitization to CS, and there was a relationship between CS and the development of chronic pain as discussed on the duration of the condition. Hence, CS is a key step on the pathway to chronic pain in those with shoulder pain, and the rehabilitation plan of shoulder injury should concentrate on early recovery.[3],[22]

The current study attempted to find if there is any association between the quantitative measures of pain and CS so that a clinical defining criterion could be identified for the diagnosis. Previous studies have reported on the evidence of identifying CS using algometer as a tool.[23],[24] In the current study, the association between the measure of CS using CSI with other objective measures such as pressure algometry in different sites of the body (PPT) revealed that PPT of tibialis anterior region of ipsilateral and contralateral legs was statistically significant, indicating a positive association with CSI score, i.e., reduced threshold for higher CSI score. Although thermal and mechanosensitivity of pain sensitization have been reported in literature previously, one literature reports lower threshold for trigger points in muscles around the shoulder girdle for patients suffering from shoulder pathology. However, the study was not done in large population to extrapolate the findings on the usage of pressure sensitivity.[25] However, the method of the conduct of the study supported the usage of pressure algometer as a valid tool; hence, for this study, we used pressure algometer for assessing the mechanosensitivity underlying CS. In the present study, the mean algometry scores for affected shoulder were lesser than the normal with higher standard deviation. Correlation analyses between CSI and pressure algometry on the TA suggest significant relation in the affected shoulder for CS [Table 3].

The study also aimed to identify the extent to which the central nervous system sensitization correlates with other clinical measures. In the current study, the CSI score had mild correlation with the demographic and clinical outcome measures and comorbidities such as gender, duration of the condition, hypertension, sleep disturbance, numbness and fatigue perception by the patients, and pain and disability scores of the shoulder [Table 3]. The mean difference for pain, disability, and duration of the condition for SPADI was also statistically different for the CS-present and no CS group of shoulder pain patients [Table 5]. The risk ratio for sensitization was 2.400 for female gender, 3.074 for hypertension, 3.198 for sleep disturbance, 2.067 for numbness, and 3.87 for perceived fatigue [Table 4]. In the subgroup of patients in this selected sample, those who are female and hypertensive are more likely to exhibit characteristics of higher pain sensitivity for shoulder pain. There were only weak evidences to support or contradict the results of the current study.[19],[26],[27] The SEM with observed variables such as endogenous (CSI score) and exogenous (duration of condition, hypertension, sleep, numbness, fatigue, and SPADI total pain) as shown in [Figure 2] revealed a fit model with Chi-square/degrees of freedom 1.270, with P = 0.211, and root mean square error of approximation of 0.05. The exogenous variables controlled 27.3% variance change in CSI scores, similar to the results discussed previously on hypertension and duration of symptoms [Table 7]. The regression estimates are shown in [Table 6] for all the exogenous variables to quantify the results, which may contribute a little in the determination and detection of subgroup of patients in unilateral shoulder pain, however with individual variation in the actual influence.{Table 7}{Table 6}

The main limitations of the present study were that there were no control group and less sample size in the context of SEM modeling analysis. However, the presence of CS in the subgroup of shoulder pain patients may have good clinical implication during the application of physiotherapeutic interventions. Further, more studies with low risk of bias and also equally involving objective variables such as PPT and variables with relatively milder influence such as duration of symptoms and hypertension are necessary for providing definite proof of the clinical importance of CS.

  Conclusion Top

The present study showed that the central nervous system becomes hypersensitive in a subgroup of patients and weakly related to factors such as female gender, chronicity of shoulder pain, hypertension, pain and disability, sleep disturbance, and perceived fatigue in patients with unilateral musculoskeletal shoulder pain.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]

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