INTRODUCTION
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has spread explosively throughout the region. The result was a new respiratory pandemic known as coronavirus 2019 (COVID-19).[1] As of March 2020, the viral infection had affected at least 192 countries, killing about 2.5 million and infecting more than 112 million.[2] However, most patients who become infected with SARS-CoV-2 were asymptomatic or have mild symptoms, but some patients developed severe symptoms that can permanently impair their quality of life.[34]
There are direct and indirect effects of this infection on several systems and organs, including neurologic, hepatic, gastrointestinal, cardiac, dermatologic, endocrine, renal and musculoskeletal systems.[56] Epidemiological data from the SARS epidemic from 2002 to 2004 identified myalgia, muscle dysfunction, osteoporosis and osteonecrosis as common complications in patients with moderate-to-severe disease.[2] Studies have shown how systemic inflammation may play a role in bone and joint pathology.[57] As a result, it is important for the treatment system to better understand and evaluate the musculoskeletal symptoms and manifestations of people with COVID-19. Preliminary studies have shown that some patients with COVID-19 also have significant musculoskeletal disorders, especially in the hip and spine, although long-term follow-up studies have not been performed.[578]
Adhesive capsulitis (AC) or joint adhesion is one of the most common causes of shoulder pain and disability.[910] In this disease, the shoulder becomes painful, and its range of motion is significantly reduced.[11] Frozen shoulder is characterised by shoulder pain and stiffness with decreased active and passive range of motion and may severely impair a person's quality of life. Coronavirus seems to have a major impact on physical activity behaviours and, consequently, the anatomical structures of the body, including the muscular system.[711] Although AC, also known as frozen shoulder, is a common and debilitating shoulder disease, its cause remains largely unknown. Its prevalence is reported to be 2%–5%. It is more common in adults aged 40–70 years old, but the reported ages are between 27 and 85 years old.[12] In a study by Sarasua et al., the 1-year prevalence of AC was reported to be about 0.35% among adults 65 years and older, which means approximately 142,000 adults in the United States.[1213] In terms of orthopaedics, frozen shoulder is a multifactorial disease that can be caused by immunology, biomechanics, endocrine as well as inflammatory diseases and leads to chronic inflammation and fibrosis. It has also been linked to immune diseases such as diabetes and thyroid diseases. In addition, depression or anxiety has been shown to affect frozen shoulder development.[14] Following COVID-19 infection, more patients in more advanced stages of AC are diagnosed.[13] Given these logical considerations, it seems that COVID-19 infection with extrapulmonary manifestations in susceptible individuals is likely to lead to the development of frozen shoulder due to immunological mechanisms. For this reason, the possibility of more detection of frozen shoulder among people with COVID-19 arises. Therefore, this study was performed to investigate the relationship between the onset of frozen shoulder and COVID-19.
MATERIALS AND METHODS
This study was a cross-sectional study. This study was ethically approved by the institutional ethics committee (IR.UMSHA.REC.1400.543). This study followed ethical standards delineated in the Helsinki declaration 1975, with an update in 2013.
Patients with AC diagnoses were enrolled in the study from September 2020 to February 2022. The diagnosis was made by a shoulder fellowship orthopaedics surgeon in a shoulder clinic. After clinical and radiological examinations, all patients with frozen shoulders who completed the consent form entered into the study. Inclusion criteria included patients with limitation of passive range of motion of the shoulder in at least two directions and a normal standard anteroposterior and lateral radiography. Exclusion criteria were history of recent shoulder trauma, rotator cuff tear, glenohumeral osteoarthritis, cervical and rheumatic injuries and/or autoimmunity at the time of examination. Demographic data, history of COVID-19 infections, time of onset of shoulder pain related to COVID-19 infection and the severity of COVID-19 were recorded. Severities of the disease were measured according to the self-reported history of hospitalisation following COVID-19 infection. All comorbidities were evaluated as potential risk factors for AC. Shoulder range of motion was assessed as passive in terms of forwarding flexion and internal and external rotation (arm next to body and elbow at 90°). The visual analogue scale (VAS) was also used to assess pain intensity. Patients were divided into two groups (with or without COVID-19 involvement), and all findings were compared between the two groups. Statistical analyses: SPSS (IBM SPSS Statistics 23) software was used for analysis; Chi-square test for qualitative data analysis and a t-test for quantitative data were used.
RESULTS
During a 6-month study period, 72 patients with a diagnosis of frozen shoulder included in the study, and 18 patients (25%) with a diagnosis of a frozen shoulder had a history of COVID-19. The results of analysis based on t test and chi showed that there was no significant difference between the two groups (frozen shoulder patients with COVID 19 with and without) this study demonstrated no significant difference in terms of gender, occupation or dominant hand (P > 0.05). Regarding the history of the disease, there was no significant difference between the two groups in terms of the history of diabetes, thyroid, history of depression and anxiety (P > 0.05). There was a significant difference between the two groups in terms of physical activity and age grouping [Table 1].
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Table 1: Baseline and clinical characteristics of patients with frozen shoulder
Information about the age, affected hand, dominant hand and range of motion, as well as the amount of pain, is given in Table 2 for a group with frozen shoulder and COVID-19. The results showed that only 5 patients with frozen shoulder who demonstrated shoulder pain after COVID-19 involvement, were male and the rest were female. All but one of them had the involvement of one shoulder. COVID-19 involvement was asymptomatic in six patients and diagnosed with positive PCR test but the rest of the patients had moderate symptoms. All patients had limitations of forwarding flexion of the shoulder and reported progression of restriction to internal and external rotation, respectively. In the pain report based on the VAS scale, the mean pain was 7.333 ± 1.608.
Table 2: Clinical data of the study sample
The pain time and severity of pain were evaluated in the both groups [Table 3]. The results showed that the severity of pain was higher in people with COVID-19 and there was a significant difference between people with and without COVID-19 (P < 0.01). Furthermore, regarding the duration of treatment in terms of months, it showed that people with COVID-19 were referred to a doctor in a shorter period of time after the beginning of the shoulder symptoms and there was a significant difference in terms of the time of referral and pain relief between the two groups (P < 0.01).
Table 3: Pain and severity of pain
DISCUSSION
This study evaluated the relationship between frozen shoulder and COVID-19 during a 6-month period during the COVID-19 pandemic. AC is a kind of inflammatory shoulder disease, which is associated with overexpression of inflammatory cytokines, the onset of pathology in AC is characterized by mglenohumeral inflammation followed by synovial and joint fibrosis.[15]
The primary pathological process in AC is known as synovial inflammation associated with vascular hyperplasia.
Little is known about joint involvement, and there is no data on synovial tissue inflammation or joint fibrosis related to COVID-19.[16] Given the association between the incidence of COVID-19 and frozen shoulder, the hypothesis is that viral disease has a direct and indirect effect on AC pathology.[15] This complication is more common in adults 40–70 years old, but the reported ages are between 27 and 85 years old.[121718] In this study, there was a significant difference between the two groups regarding the age range of frozen shoulder (P < 0.039). Claudio Ascani et al. reported mean age of 57 years, which is in the age range of 50–70 years.
In our study, all patients had limitations in range of motion in forwarding flexion, internal rotation and external rotation in affected hands. Although there is no statistically significant difference between the two groups, but people who suffered from frozen shoulder after covid-19 referred to a specialist in a shorter time and also intensity of pain in patients with covid -19 involvement was significantly higher(P < 0.005) than patients without covid-19 involvement [Table 2]. This is in contrast to our primary hypothesis that frozen shoulder may be more frequent and more severe in patients with covid -19 as the patient may have delay to start treatment. We hypothesize that both direct and indirect effects of viral disease may play a role in its development. The prevalence of frozen shoulder is reported to be 2%–5%.[18] The results showed that there was no significant difference between the two groups in terms of the history of diabetes, thyroid disease, depression and anxiety.
In this study, the results showed that there is a significant difference between the two groups in terms of physical activity. So that 24.78% of frozen shoulder patients with COVID-19 involvment and 57.41%of patientsof frozen shoulder without COVID-19 involvement had a history of regular physical activity. A study of Sallis et al. demonstrated that regular physical activity is related to lower risk of COVID-19 complications.[19] Regular physical activity reduces the risk of systemic inflammation, which is a major cause of COVID-19-induced lung damage.[20]
In the study of Claudio Ascani et al., frozen shoulders were diagnosed 2 months after the beginning of the symptoms. In our study, patients were referred to the shoulder clinic later, and there was a significant difference between the two groups so that patients without COVID-19 infection were referred earlier (4.388 ± 3.36) related to patients without COVID-19 infection (10.444 ± 9.64). This may be due to late coming of patients with shoulder problems to medical centers due to fear of getting COVID-19 in that centers.
Regarding the severity of COVID-19 disease, out of 18 patients, 6 (33.33%) were asymptomatic, and the rest were moderately COVID-19.
Our study included patients referred to the outpatient clinic, but Álvarez et al. showed that people admitted to the intensive care unit (ICU) following COVID-19 had shoulder pain.[21] Therefore, individuals should be evaluated for shoulder pain and changes in ICUs based on these results. Shoulder pain (5%–80%) persisted in patients 6–12 months after discharge.[2122] Although patients who are admitted to the ICU unit may take corticosteroids and it may affect the incidence and symptoms of AC, in our study, there was no history of admission and corticosteroid administration. Musculoskeletal disorders, especially shoulder pain, affect the quality of life.[22] Pain affects the function of the upper extremities and imposes high costs on the community health system.[2223]
Only one of the AC patients with COVID-19 involvement had simultaneous bilateral shoulder involvement (5.5%) As bilateral simultaneous involvement of the shoulders in AC could be observed in 14% of the patients.[24] It seems that COVID-19 involvement does not increase the incidence of bilateral involvement of the shoulders.
Studies show that the inflammatory response in AC is very similar to COVID-19 and that synovial cells may be targeted by SARS-CoV-2.[22] Based on this study, we hypothesised that COVID-19 might lead to AC in the shoulder. Therefore, it is recommended to conduct this study in the wider community, and in case of the high incidence of frozen shoulder in COVID-19 patients, it can pave the way for an analytical study to determine the effect of COVID-19 disease and the occurrence of frozen shoulder.
CONCLUSION
COVID-19-infected patients may experience frozen shoulder at a younger age and more severe shoulder pain. Delay in referring to medical centre does not seem to have a role in the incidence of frozen shoulder in these patients and direct effect of the disease may be the main problem. Regular physical activity is an important prognostic factor for severity of frozen shoulder in these patients.
Ethics statement
IR.UMSHA.REC.1400.543.
Financial support and sponsorship
The study was funded by the Vice-chancellor for Research and Technology, Hamadan University of Medical Sciences (No. 140007276005).
Conflicts of interest
There are no conflicts of interest.
Acknowledgements
This study was adapted from an MSc thesis at Hamadan University of Medical Sciences.
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