Increased Risk for Adhesive Capsulitis of the Shoulder following Cervical Disc Surgery

Shoulder problems are common in patients with a cervical herniated intervertebral disc (HIVD). This study aimed to explore the incidence and risk of shoulder capsulitis/tendonitis following cervical HIVD surgery. We used data from the Taiwan “Longitudinal Health Insurance Database”. We identified all patients who were hospitalized with a diagnosis of displacement of a cervical HIVD and who underwent cervical surgery (n = 1625). We selected 8125 patients who received cervical HIVD conservative therapy only as the comparison group matched with study patients. We individually tracked these sampled patients for 6 months to identify all patients who received a diagnosis of shoulder tendonitis/capsulitis. We found that incidence rates of shoulder tendonitis/capsulitis during the 6-month follow-up period were 3.69 (95% CI: 2.49~5.27) per 100 person-years for the study group and 2.33 (95% CI: 1.89~2.86) per 100 person-years for the comparison group. Cox proportional hazard regressions showed that the adjusted hazard ratio for shoulder tendonitis/capsulitis among patients who underwent cervical disc surgery was 1.66 (95% CI = 1.09~2.53) when compared to comparison group. We concluded that patients who underwent surgery for a cervical HIVD had a significantly higher risk of developing shoulder capsulitis/tendonitis in 6 months follow-up compared to patients who received cervical HIVD conservative therapy only.

Scientific RepoRts | 6:26898 | DOI: 10.1038/srep26898 following surgery for a cervical HIVD in a large population-based study. The data are critical for developing adequate clinical management and providing a fundamental basis for postoperative management.

Methods
Database. This study used data sourced from the "Longitudinal Health Insurance Database 2005 (LHID2005)" released by the Taiwan National Health Research Institute (NHRI) in 2006. Taiwan began a single-payer National Health Insurance (NHI) program in 1995 to provide affordable health care for all of the island's residents. The LHID2005 contains all medical claims data for 1,000,000 beneficiaries, randomly sampled from all enrollees (n = 25.68 million) covered under the NHI program. The Taiwan NHRI reports that there were no statistically significant differences in the distributions of age, gender, or healthcare costs between patients in the LHID2005 and all enrollees. Therefore, the LHID2005 provides a unique opportunity to examine the risk of shoulder capsulitis/tendonitis in patients who had undergone surgery for a cervical HIVD. Study Sample. This study consisted of a study group and a comparison group. We identified all patients who were hospitalized with a diagnosis of displacement of a cervical intervertebral disc (ICD-9-CM code 722.0) and underwent cervical fusion, anterior technique (ICD-9-CM procedure code 810.2) or excision of the intervertebral disc (ICD-9-CM procedure code 805.1) between January 1, 2001 and December 31, 2013 (n = 1661). We defined the date of undergoing cervical disc surgery as the index date for the study group. We then excluded patients who were less than 18 years old in order to limit our study sample to the adult population (n = 1). Furthermore, in order to increase the likelihood of identifying only new shoulder tendonitis/capsulitis cases, we excluded 35 patients who had ever received a diagnosis of shoulder tendonitis/capsulitis (ICD-9-CM codes 726.0, 726.1, or 726.2) within 6 months prior to the index date. Finally, 1625 patients were included in the study group.
As for comparison group, we first identified 17,391 patients who received a first-time diagnosis of displacement of a cervical intervertebral disc (ICD-9-CM code 722.0) in ambulatory care centers or hospitalizations between 1 January 2001 and 31 December 2013. We designated the date of receiving their first-time diagnosis of cervical HIVD as index date for comparison group. We then excluded those patients who had ever undergone cervical disc surgery after the index date. Thereafter, using the SAS proc surveyselect program, we randomly extracted 8,125 comparison patients (five for every patient who underwent a cervical disc surgery) from the remaining patients matched with the study patients in terms of gender, age group (18~40, 40~49, 50~59, 60~69, and > 69 years), and index year. We also assured that none of the selected comparison patients had ever received a diagnosis of shoulder tendonitis/capsulitis within 6 months prior to the index date. Ultimately, we individually tracked these sampled patients (n = 9750) for 6 months from their index date to identify all patients who subsequently received a diagnosis of shoulder tendonitis/capsulitis during the follow-up period.
Statistical Analysis. We used the SAS statistical package (SAS System for Windows, vers. 8.2) to perform all statistical analyses. Pearson χ 2 tests and t-tests were used to explore differences in sociodemographic characteristics (age, sex, monthly insured income amount, and geographic region and level of urbanization of the community in which the patient resided) between the study and comparison groups. Cox proportional hazard regressions, which do not invoke proportionality assumptions, were used to calculate the hazard of shoulder tendonitis/capsulitis between these two groups. A two-sided p value of ≤ 0.05 was considered significant in this study. Table 1 shows the distribution of sociodemographic characteristics between patients who underwent cervical disc surgery and the comparison group. There was no significant difference in the mean age between these two groups (p = 0.165). Pearson χ 2 tests revealed that patients who underwent cervical disc surgery were more likely to reside in the northern part of Taiwan (p < 0.001) than patients in the comparison group. Table 2 shows the distribution of shoulder tendonitis/capsulitis during the 6-month follow-up period between patients who underwent cervical disc surgery and comparison patients. We found that of the total sample of 9750 patients, 125 patients (1.28%) subsequently received a diagnosis of shoulder tendonitis/capsulitis during the 6-month follow-up period, 30 (1.85% of the patients who underwent a cervical disc surgery) from the study group and 95 (1.17% of patients in the comparison group) from the comparison group. Incidence rates of shoulder tendonitis/capsulitis during the 6-month follow-up period were 3.69 (95% CI: 2.49~5.27) per 100 person-years for the study group and 2.33 (95% CI: 1.89~2.86) per 100 person-years for the comparison group. The log-rank test indicated that there was a significant difference in shoulder tendonitis/capsulitis-free survival rates between patients who underwent cervical disc surgery and comparison patients (p = 0.002). Table 3 shows the crude and adjusted hazard ratios (HRs) of shoulder tendonitis/capsulitis within the 6-month follow-up period comparing patients who underwent cervical disc surgery and comparison patients. The crude HR for shoulder tendonitis/capsulitis for patients who underwent cervical disc surgery was 1.59 (95% CI = 1.05~2.41) compared to comparison patients. Furthermore, the HR for shoulder tendonitis/capsulitis for patients who underwent cervical disc surgery was 1.66 (95% CI = 1.09~2.53) times higher over the 6-month follow-up period, after adjusting for monthly income, level of urbanization of the community and geographic region in which the patient resided.

Results
We have further analyzed the risk of tendonitis/capsulitis during the 1-year follow-up period. We found that the HR for shoulder tendonitis/capsulitis for patients who underwent cervical disc surgery was 1.56 (95% CI = 1.10~2.21) times higher over the 1-year follow-up period. The relationship between cervical disc surgery and shoulder tendonitis/capsulitis still sustained even during the 1-year follow-up period.

Discussion
We found an increased risk for shoulder capsulitis and tendonitis in the population with a cervical HIVD following cervical surgery in a large population-based cohort study. The adjusted HR for developing shoulder capsulitis/ tendonitis following cervical surgery was 1.66 compared to patients who received cervical HIVD conservative therapy only. Although the overall prevalence of shoulder capsulitis/tendonitis was relatively minor (1.85% in patients who received cervical HIVD surgery), there are significant numbers of patients receiving cervical surgery for HIVD annually. Therefore, recognition of this issue can improve patient management and satisfaction following cervical surgery for an HIVD.
Even though the concept regarding an association between cervical and shoulder disorders has been noted for a long time, epidemiological data are still very limited. A study showed more evidence of degenerative changes at C5/6 and C6/7 intervertebral discs in patients with shoulder capsulitis/tendonitis than a control population 6 . However, that cross-sectional study was limited in being unable to establish a temporal association between the two conditions. Another observational case series study noted an increased prevalence of shoulder periarthritis/ capsulitis following cervical surgery for an HIVD 6 . However, the overall risk of shoulder capsulitis/tendonitis following cervical surgery could not be estimated in this study since it lacked a control population. To our best knowledge, the present investigation is the first study to explore the prevalence and risk of developing shoulder capsulitis/tendonitis following surgery for a cervical HIVD with a large population cohort. Our study can add knowledge of this issue and should be useful in providing adequate patient information and facilitate postoperative care in this population.
The mechanisms of a "paradoxically" increased risk of shoulder capsulitis/tendonitis following cervical surgery may be complex. To our best knowledge, there is very scanty data to indicate and explore the pathomechanism of the association between cervical HIVD surgery and postoperative shoulder capsulitis. Therefore, we can only raise several hypotheses in present study based on current available works and observations. First, relative immobilization and reduced movements of the neck and shoulder region following surgery may increase the risk of developing shoulder capsulitis 7 Table 2. Relationships of cervical disc surgery with shoulder tendonitis/capsulitis during the 6-month follow-up period for patients who underwent cervical disc surgery and comparison patients (n = 9750). CI, confidence interval.
few patients may have arm palsy or weakness following cervical decompression surgery for an HIVD which is known as C5 palsy syndrome 8,9 . The cause of C5 palsy syndrome is still not well understood, and multiple factors were proposed to be associated with C5 palsy syndrome, such as direct C5 root injury, root tethering, spinal cord ischemia, reperfusion injury, and segmental spinal cord disease 9 . Patients with C5 palsy syndrome present remarkable weakness involving muscles innervated by the C5 root. Although most patients with C5 palsy syndrome gradually recover postoperatively, temporary shoulder girdle weakness and dysfunction may put patients at high risk of developing postoperative shoulder capsulitis/tendonitis. Third, successful cervical decompression surgery may lead to significant pain relief which may allow patients to increase the functional use of their upper extremities in their daily activities following surgery. The increased daily upper extremity use may contribute to a risk of overuse and injury of the shoulder. Nevertheless, further study is still need to verify these hypotheses. Shoulder capsulitis/tendonitis is a common musculoskeletal problem in the general population. The shoulder is the most mobile joint of the body and is critical to performing upper extremity functions. Although most cases of shoulder capsulitis/tendonitis can successfully be treated, shoulder capsulitis/tendonitis can still be associated with pain and disability for a considerable period and an increased medical burden 10 . The increased risk of shoulder capsulitis/tendonitis may be preventable following cervical surgery for a cervical HIVD. Several steps should be considered. Careful preoperative evaluation of shoulder mobility and the functional status is helpful in differentiating some patients with comorbid shoulder capsulitis/tendonitis. Intensive treatment of comorbid shoulder problems prior to surgery can optimize postoperative outcomes and improve patient satisfaction. Patients who undergo cervical surgery should be instructed about an adequate mobilization program of the shoulders. A strengthening program of the shoulder girdle should be emphasized for patients with C5/6 radiculopathy and/or shoulder muscle weakness.
Aggressive pain control following surgery is fundamental. Inadequate pain control can promote immobilization and further loss of function. Careful monitoring of the shoulder's range of motion and function postoperatively is necessary. Early detection and aggressive management of shoulder capsulitis/tendonitis are linked to better outcomes and prevention of functional loss. Neurological recovery in patients with cervical radiculopathy could be timely and incomplete even after successful surgical decompression of the cervical roots. Prolonged cervical radiculopathy may cause weakness and dysfunction of the shoulder girdle which can promote shoulder capsulitis. For patients with severe radiculopathy preoperatively or C5 palsy syndrome postoperatively, preventive rehabilitation may be needed to minimize immobilization and inactivity of the shoulder.
Limitations of present study should be addressed. First, shoulder capsulitis/tendonitis may have been mis-coded or uncoded in the registry-based database, particularly of patients who had minor symptoms and did not seek medical services. In addition, some shoulder symptoms may mimic radicular pain which may have been undiagnosed preoperatively in patients with comorbid shoulder capsulitis/tendonitis. Second, the neurological status and level of patients who underwent cervical HIVD surgery could not be determined from the database. In theory, patients with more-severe cervical radiculopathy involving C5/6 may have a higher risk of developing shoulder problems. Third, some variables such as occupation, trauma history, family history, physical activity, cigarette smoking, and obesity which may have confounded our findings could not be determined in the present study. Fourth, we did not analyze the effects by the surgery types for cervical HIVD. Complications of cervical spine surgery are usually dependent on the type of procedure. The risk for developing shoulder capsulitis/tendonitis may vary with different types of surgery. Finally, the causes of cervical HIVD could not be determined in our database. Degenerative and traumatic HIVDs may be associated with different risks of developing shoulder capsulitis/tendonitis.

Conclusions
Patients who underwent surgery for a cervical HIVD had a higher risk of subsequently developing shoulder capsulitis/tendonitis postoperatively compared to patients who received cervical HIVD conservative therapy only in 6 months follow-up in a large population-based cohort study. Adequate monitoring and management of shoulder problems in patients with a cervical HIVD surgery are suggested.