Can adhesive capsulitis of the shoulder be a consequence of COVID-19? Case series of 12 patients
2021; Elsevier BV; Volume: 30; Issue: 7 Linguagem: Inglês
10.1016/j.jse.2021.04.024
ISSN1532-6500
AutoresClaudio Ascani, Daniele Passaretti, Marco Scacchi, Gianluca Bullitta, Mauro De Cupis, Monia Pasqualetto, Jacopo Ascani,
Tópico(s)Intramuscular injections and effects
ResumoSevere acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) has spread explosively throughout the world, resulting in a pandemic new respiratory disease identified as coronavirus disease 2019 (COVID-19). Since March 2020, the viral infection has affected at least 192 countries or regions, causing about 2.5 million deaths and infecting more than 112 million people.25Johns Hopkins UniversityCoronavirus resource center.https://coronavirus.jhu.eduDate accessed: February 22, 2021Google Scholar Patients with COVID-19 can be classified into 3 groups according to the severity of the viral infection: (1) asymptomatic and mild COVID-19 patients, who account for the majority of cases (approximately 80%), (2) severely ill patients (14%), and (3) critical patients (6%).13Guan W.J. Ni Z.Y. Hu Y. Liang W.H. Ou C.Q. He J.X. et al.China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China.N Engl J Med. 2020; 382: 1708-1720https://doi.org/10.1056/NEJMoa2002032Crossref PubMed Scopus (20397) Google Scholar,43Wu Z. McGoogan J.M. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention.JAMA. 2020; 323: 1239-1242https://doi.org/10.1001/jama.2020.2648Crossref PubMed Scopus (12697) Google Scholar COVID-19 symptoms differ in the 3 groups.43Wu Z. McGoogan J.M. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention.JAMA. 2020; 323: 1239-1242https://doi.org/10.1001/jama.2020.2648Crossref PubMed Scopus (12697) Google Scholar Patients with mild symptoms generally suffer from nasal congestion, fever, anosmia and dysgeusia, a sore throat, cough, headache, malaise, and myalgia. Patients with a severe presentation frequently require hospitalization owing to pneumonia and acute respiratory distress syndrome. The symptoms in critical patients include respiratory failure, septic shock, multiorgan dysfunction syndrome, and disseminated intravascular coagulation.43Wu Z. McGoogan J.M. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention.JAMA. 2020; 323: 1239-1242https://doi.org/10.1001/jama.2020.2648Crossref PubMed Scopus (12697) Google Scholar Systemic manifestations of COVID-19 result from a combination of the direct effects of the SARS-CoV-2 on infected target cells and of the indirect effects due to the host's inflammatory response to the virus. In particular, the indirect effects are associated with a cytokine storm and a systemic inflammation that involve any organ or system, including the musculoskeletal system.4Cheng H. Wang Y. Wang G.Q. Organ-protective effect of angiotensin-converting enzyme 2 and its effect on the prognosis of COVID-19.J Med Virol. 2020; 92: 726-730https://doi.org/10.1002/jmv.25785Crossref PubMed Scopus (344) Google Scholar,21Huang C. Wang Y. Li X. Ren L. Zhao J. Hu Y. et al.Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020; 395: 497-506https://doi.org/10.1016/S0140-6736(20)30183-5Crossref PubMed Scopus (33065) Google Scholar The main musculoskeletal manifestations that as of this writing have been associated with COVID-19 are myalgias and generalized weakness, which are reported as early, transient features in 15%-45% of symptomatic patients and resolve on average within 10-15 days.19Heydari K. Rismantab S. Shamshirian A. Lotfi P. Shadmehri N. Houshmand P. et al.Clinical and paraclinical characteristics of COVID-19 patients: a systematic review and meta-analysis.medRxiv. 2020; https://doi.org/10.1101/2020.03.26.20044057Crossref Scopus (0) Google Scholar,34Nasiri M.J. Haddadi S. Tahvildari A. Farsi Y. Arbabi M. 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De Micheli A.J. Schonk M.M. Konnaris M.A. Piacentini A.N. Edon D.L. et al.Musculoskeletal Consequences of COVID-19.J Bone Joint Surg Am. 2020; 102: 1197-1204https://doi.org/10.2106/JBJS.20.00847Crossref PubMed Scopus (230) Google Scholar,21Huang C. Wang Y. Li X. Ren L. Zhao J. Hu Y. et al.Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020; 395: 497-506https://doi.org/10.1016/S0140-6736(20)30183-5Crossref PubMed Scopus (33065) Google Scholar Less is known about joint symptoms, with no studies having yet been published on inflammation of the synovial tissue or joint fibrosis related to COVID-19. Among the inflammatory diseases involving the shoulder and associated with an overexpression of inflammatory cytokines is adhesive capsulitis (AC).28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar Described for the first time in 1872 by Duplay9Duplay S. Scapulo-humeral periarthritis and shoulder stiffness resulting from it..Arch Gen Med. 1872; 20 ([in French]): 513-542Google Scholar and subsequently also defined as frozen shoulder by Codman,5Codman E.A. The shoulder. Rupture of the supraspinatus tendon and other lesions in or about the subacromial bursa. Thomas Todd, Boston1934: 216-224Google Scholar AC is characterized by shoulder pain and stiffness combined with reduced active and passive range of motion and may severely impair a person's quality of life. Several studies16Hand G.C. Athanasou N.A. Matthews T. Carr A.J. The pathology of frozen shoulder.J Bone Joint Surg Br. 2007; 89: 928-932https://doi.org/10.1302/0301-620X.89B7.19097Crossref PubMed Scopus (278) Google Scholar,26Kanbe K. Inoue K. Inoue Y. Chen Q. Inducement of mitogen-activated protein kinases in frozen shoulders.J Orthop Sci. 2009; 14: 56-61https://doi.org/10.1007/s00776-008-1295-6Abstract Full Text PDF PubMed Scopus (44) Google Scholar,28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar,33Nago M. Mitsui Y. Gotoh M. Nakama K. Shirachi I. Higuchi F. et al.Hyaluronan modulates cell proliferation and mRNA expression of adhesion-related procollagens and cytokines in glenohumeral synovial/capsular fibroblasts in adhesive capsulitis.J Orthop Res. 2010; 28: 726-731https://doi.org/10.1002/jor.21075Crossref PubMed Scopus (29) Google Scholar,36Rodeo S.A. Hannafin J.A. Tom J. Warren R.F. Wickiewicz T.L. Immunolocalization of cytokines and their receptors in adhesive capsulitis of the shoulder.J Orthop Res. 1997; 15: 427-436Crossref PubMed Scopus (277) Google Scholar have shown that the beginning of the pathologic process in AC is characterized by a glenohumeral inflammation followed by synovial and periarticular fibrosis.16Hand G.C. Athanasou N.A. Matthews T. Carr A.J. The pathology of frozen shoulder.J Bone Joint Surg Br. 2007; 89: 928-932https://doi.org/10.1302/0301-620X.89B7.19097Crossref PubMed Scopus (278) Google Scholar,26Kanbe K. Inoue K. Inoue Y. Chen Q. Inducement of mitogen-activated protein kinases in frozen shoulders.J Orthop Sci. 2009; 14: 56-61https://doi.org/10.1007/s00776-008-1295-6Abstract Full Text PDF PubMed Scopus (44) Google Scholar,28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar,33Nago M. Mitsui Y. Gotoh M. Nakama K. Shirachi I. Higuchi F. et al.Hyaluronan modulates cell proliferation and mRNA expression of adhesion-related procollagens and cytokines in glenohumeral synovial/capsular fibroblasts in adhesive capsulitis.J Orthop Res. 2010; 28: 726-731https://doi.org/10.1002/jor.21075Crossref PubMed Scopus (29) Google Scholar,36Rodeo S.A. Hannafin J.A. Tom J. Warren R.F. Wickiewicz T.L. Immunolocalization of cytokines and their receptors in adhesive capsulitis of the shoulder.J Orthop Res. 1997; 15: 427-436Crossref PubMed Scopus (277) Google Scholar Based on reports that the inflammatory reaction in AC28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar,36Rodeo S.A. Hannafin J.A. Tom J. Warren R.F. Wickiewicz T.L. Immunolocalization of cytokines and their receptors in adhesive capsulitis of the shoulder.J Orthop Res. 1997; 15: 427-436Crossref PubMed Scopus (277) Google Scholar shows several similarities to that in COVID-19, and that synovial cells may be targeted by the SARS-CoV-2,6De Micheli A.J. Spector J.A. Elemento O. Cosgrove B.D. A reference single-cell transcriptomic atlas of human skeletal muscle tissue reveals bifurcated muscle stem cell populations.Skelet Muscle. 2020; 10: 19https://doi.org/10.1186/s13395-020-00236-3Crossref PubMed Scopus (90) Google Scholar,23Ji Q. Zheng Y. Zhang G. Hu Y. Fan X. Hou Y. et al.Single-cell RNA-seq analysis reveals the progression of human osteoarthritis.Ann Rheum Dis. 2019; 78: 100-110https://doi.org/10.1136/annrheumdis-2017-212863Crossref PubMed Scopus (216) Google Scholar,40Sun H. Wen X. Li H. Wu P. Gu M. Zhao X. et al.Single-cell RNA-seq analysis identifies meniscus progenitors and reveals the progression of meniscus degeneration.Ann Rheum Dis. 2020; 79: 408-417https://doi.org/10.1136/annrheumdis-2019-215926Crossref PubMed Scopus (65) Google Scholar,46Zhang F. Wei K. Slowikowski K. Fonseka C.Y. Rao D.A. Kelly S. et al.Defining inflammatory cell states in rheumatoid arthritis joint synovial tissues by integrating single-cell transcriptomics and mass cytometry.Nat Immunol. 2019; 20: 928-942https://doi.org/10.1038/s41590-019-0378-1Crossref PubMed Scopus (655) Google Scholar we hypothesized that COVID-19 might be related to the development of AC in the shoulder. Here, we present our case series of patients with AC evaluated at our hospital. The study group included 12 consecutive, prospectively enrolled, subjects with AC. The diagnosis, which was made by the senior author (C.A.) after clinical and radiologic examination, was based on a reduction in both active and passive range of motion (ROM) of the shoulder, evaluated in the sitting and supine positions; no strength reduction in intra-extrarotation; exclusion of the posterosuperior18Hertel R. Ballmer F.T. Lombert S.M. Gerber C. 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American Academy of Orthopaedic Surgeons, Rosemont, IL1997: 135Google Scholar rotator cuff tendon tears; a radiographic evaluation, that is, true anteroposterior view (with the central ray tangential to the glenoid surface) and a Velpeau axillary view (with the patient's arm held in internal rotation, the ray is superior to inferior and the patient leaning backward); and an MRI of the involved shoulder. All the patients were evaluated between November 15, 2020, and January 15, 2021, at the shoulder surgery unit at our hospital, and all reported shoulder stiffness and pain arising after COVID-19, with no apparent cause. At the time of our examination, none of the patients enrolled reported the following: a recent shoulder trauma; previous diagnosis of AC in either shoulder; a previous ROM limitation or a rotator cuff tear; severe glenohumeral osteoarthritis; cervical spine symptoms and rheumatologic and/or autoimmune pathologies. The total number of patients and those with AC evaluated during the study period were noted. Clinical information on gender, age, affected side, time of AC onset after COVID-19 diagnosis, severity of COVID-19, shoulder functional limitation, and pain intensity was recorded. All comorbidities, as possible risk factors for development of AC, were noted. Passive shoulder ROM was evaluated in terms of forward elevation, abduction, and external rotation (with the arm at the side and elbow flexed at 90°). The visual analog scale (VAS) was used to assess pain intensity.22Jensen M.P. Karoly P. Pain-specific beliefs, perceived symptom severity, and adjustment to chronic pain.Clin J Pain. 1992; 8: 123-130Crossref PubMed Scopus (111) Google Scholar All the patients signed an informed consent form in accordance with the Declaration of Helsinki. During the study period, a total of 1120 patients were evaluated at our shoulder surgery unit. Of these, 146 had an AC of the shoulder. The study sample was composed of 12 patients: 8 female and 4 male. The patients' mean age was 57 years (range: 42-73). All the clinical data are presented in Table I.Table IClinical data of the study samplePt no.SexAgeSideAC onset∗AC onset after COVID-19 diagnosis in terms of months.COVID-19 severityPassive ROM†Reduction of motion compared with the uninjured contralateral side. Values are in degrees, expressed as mean (reduction of motion compared with the uninjured contralateral side).VAS scoreFEAbdER1F73L2Mild100 (60)90 (60)10 (35)52F42R2Asymptomatic70 (110)50 (130)0 (50)83F50R2.5Asymptomatic110 (60)80 (90)10 (30)64M49L3Mild150 (25)100 (80)20 (25)45F54R3Asymptomatic140 (40)100 (75)10 (40)56F57R2Mild160 (10)130 (40)30 (10)37M59L1.5Asymptomatic70 (95)40 (120)0 (40)88F61R3Asymptomatic170 (10)150 (25)35 (15)39F65L2Mild130 (35)100 (60)15 (25)610M57Both1.5AsymptomaticR: 100; L: 110R: 90; L: 90R: 10; L: 15711M62L2.5Mild120 (50)100 (70)30 (15)512F51L2Asymptomatic80 (100)40 (140)5 (45)7Pt, patient; F, female; M, male; L, left; R, right; AC, adhesive capsulitis; ROM, range of motion; FE, forward elevation; Abd, abduction; ER, external rotation (with the arm at the side and elbow flexed at 90°); VAS, visual analog scale for pain.∗ AC onset after COVID-19 diagnosis in terms of months.† Reduction of motion compared with the uninjured contralateral side. Values are in degrees, expressed as mean (reduction of motion compared with the uninjured contralateral side). Open table in a new tab Pt, patient; F, female; M, male; L, left; R, right; AC, adhesive capsulitis; ROM, range of motion; FE, forward elevation; Abd, abduction; ER, external rotation (with the arm at the side and elbow flexed at 90°); VAS, visual analog scale for pain. The right shoulder was involved in 5 subjects and the left shoulder in 6 subjects, whereas 1 patient reported symptoms in both shoulders. AC arose 1.5-3 months after the COVID-19 diagnosis (mean time to onset: 2 months). According to severity, COVID-19 in 7 of the patients was asymptomatic, whereas in the remaining 5 patients symptoms were mild. None of the patients were severely or critical ill. As for other comorbidities, 2 patients had well-compensated diabetes mellitus. The decrease in range of motion was as follows: mean forward elevation of the affected side was 116° (range: 70°-170°), with a mean reduction compared with the uninjured shoulder of 54° (range: 10°-110°); the mean abduction was 89° (range: 40°-150°) and mean external rotation was 15° (range: 0°-35°), with a mean reduction compared with the contralateral side of 81° (range: 25°-140°) and 30° (range: 10°-50°), respectively. The mean pain intensity was 5.6 (range: 3-8). Table II shows all the mean ROM and VAS values in the patients with asymptomatic and mild-symptomatic COVID-19.Table IIROM and pain intensity in asymptomatic and mild symptomatic COVID-19 patientsPassive ROM∗Reduction of motion compared with the uninjured contralateral side. Values are in degrees, expressed as mean (reduction of motion compared with the uninjured contralateral side).VAS score, meanFEAbdERAsymptomatic patients (n = 7)106 (69)80 (97)11 (37)6.3Mild patients (n = 5)132 (36)104 (62)21 (22)4.6ROM, range of motion; FE, forward elevation; Abd, abduction; ER, external rotation (with the arm at the side and elbow flexed at 90°); VAS, visual analog scale for pain.∗ Reduction of motion compared with the uninjured contralateral side. Values are in degrees, expressed as mean (reduction of motion compared with the uninjured contralateral side). Open table in a new tab ROM, range of motion; FE, forward elevation; Abd, abduction; ER, external rotation (with the arm at the side and elbow flexed at 90°); VAS, visual analog scale for pain. The initial pathologic process in AC is known to be a synovial inflammation associated with a hypervascular hyperplasia. This is followed by fibroblast hyperactivity and subsequent fibrosis in the synovium and glenohumeral capsular tissue,28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar,36Rodeo S.A. Hannafin J.A. Tom J. Warren R.F. Wickiewicz T.L. Immunolocalization of cytokines and their receptors in adhesive capsulitis of the shoulder.J Orthop Res. 1997; 15: 427-436Crossref PubMed Scopus (277) Google Scholar located above all in the coracohumeral ligament and to the rotator interval area.2Bunker T.D. Reilly J. Baird K.S. Hamblen D.L. Expression of growth factors, cytokines and matrix metalloproteinases in frozen shoulder.J Bone Joint Surg Br. 2000; 82: 768-773Crossref PubMed Scopus (185) Google Scholar,15Hand C. Clipsham K. Rees J.L. Carr A.J. 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As regards the correlation between COVID-19 and the frozen shoulder, we hypothesize that both direct and indirect effects of the viral disease may contribute to the pathogenesis of AC. Cellular penetration of SARS-CoV-2 occurs via the angiotensin-converting enzyme 2 (ACE2) receptor and the serine protease TMPRSS2 (transmembrane protease, serine 2).20Hoffmann M. Kleine-Weber H. Schroeder S. Krüger N. Herrler T. Erichsen S. et al.SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor.Cell. 2020; 181: 271-280.e8https://doi.org/10.1016/j.cell.2020.02.052Abstract Full Text Full Text PDF PubMed Scopus (13550) Google Scholar Following receptor binding, TMPRRS2 permits mixing of human and viral membranes by proteolytic cleavage of the viral S protein, thus allowing entry into the cell of the viral RNA.10Fehr A.R. Perlman S. 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However, among these, only pericytes and smooth muscle cells express the ACE2 receptor. By contrast, several cells in the synovium, including fibroblasts and monocytes, express both ACE2 and TMPRSS2.6De Micheli A.J. Spector J.A. Elemento O. Cosgrove B.D. A reference single-cell transcriptomic atlas of human skeletal muscle tissue reveals bifurcated muscle stem cell populations.Skelet Muscle. 2020; 10: 19https://doi.org/10.1186/s13395-020-00236-3Crossref PubMed Scopus (90) Google Scholar,23Ji Q. Zheng Y. Zhang G. Hu Y. Fan X. Hou Y. et al.Single-cell RNA-seq analysis reveals the progression of human osteoarthritis.Ann Rheum Dis. 2019; 78: 100-110https://doi.org/10.1136/annrheumdis-2017-212863Crossref PubMed Scopus (216) Google Scholar,40Sun H. Wen X. Li H. Wu P. Gu M. 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Edon D.L. et al.Musculoskeletal Consequences of COVID-19.J Bone Joint Surg Am. 2020; 102: 1197-1204https://doi.org/10.2106/JBJS.20.00847Crossref PubMed Scopus (230) Google Scholar This finding may be one of the main direct effects of the SARSCoV-2 on the synovium and fibroblasts and, therefore, be related to fibrosis of the capsular and pericapsular tissues in the AC. In addition to direct infection of the cells outside of the respiratory tract, COVID-19 is characterized by indirect effects resulting from the host's response to the viral infection. These indirect effects are associated with a cytokine storm and a systemic inflammation that may impact nearly every organ system, including the musculoskeletal tissues.4Cheng H. Wang Y. Wang G.Q. Organ-protective effect of angiotensin-converting enzyme 2 and its effect on the prognosis of COVID-19.J Med Virol. 2020; 92: 726-730https://doi.org/10.1002/jmv.25785Crossref PubMed Scopus (344) Google Scholar,21Huang C. Wang Y. Li X. Ren L. Zhao J. Hu Y. et al.Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020; 395: 497-506https://doi.org/10.1016/S0140-6736(20)30183-5Crossref PubMed Scopus (33065) Google Scholar In particular, circulating levels of signaling molecules and proinflammatory cytokines, including interleukin 1 beta (IL-1b), IL-6, IL-8, IL-17, tumor necrosis factor alpha (TNF-α), granulocyte colony–stimulating factor, interferon gamma (IFN-γ), and other chemokines, are very high.21Huang C. Wang Y. Li X. Ren L. Zhao J. Hu Y. et al.Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020; 395: 497-506https://doi.org/10.1016/S0140-6736(20)30183-5Crossref PubMed Scopus (33065) Google Scholar,30Liu J. Li S. Liu J. Liang B. Wang X. Wang H. et al.Longitudinal characteristics of lymphocyte responses and cytokine profiles in the peripheral blood of SARS-CoV-2 infected patients.EBioMedicine. 2020; 55: 102763https://doi.org/10.1016/j.ebiom.2020.102763Abstract Full Text Full Text PDF PubMed Scopus (1189) Google Scholar,45Ye Q. Wang B. Mao J. The pathogenesis and treatment of the "Cytokine storm" in COVID-19.J Infect. 2020; 80: 607-613https://doi.org/10.1016/j.jinf.2020.03.037Abstract Full Text Full Text PDF PubMed Scopus (2079) Google Scholar In strong analogy with COVID-19, the inflammatory cascade implicated in abnormal tissue repair and fibrosis of the shoulder AC is supported by similar cytokines and growth factors, particularly IL-1, IL-6, and TNF-α.28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar,36Rodeo S.A. Hannafin J.A. Tom J. Warren R.F. Wickiewicz T.L. Immunolocalization of cytokines and their receptors in adhesive capsulitis of the shoulder.J Orthop Res. 1997; 15: 427-436Crossref PubMed Scopus (277) Google Scholar Moreover, several authors28Lho Y.M. Ha E. Cho C.H. Song K.S. Min B.W. Bae K.C. et al.Inflammatory cytokines are overexpressed in the subacromial bursa of frozen shoulder.J Shoulder Elbow Surg. 2013; 22: 666-672https://doi.org/10.1016/j.jse.2012.06.014Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar,32Mullett H. Byrne D. Colville J. Adhesive capsulitis: human fibroblast response to shoulder joint aspirate from patients with stage II disease.J Shoulder Elbow Surg. 2007; 16: 290-294https://doi.org/10.1016/j.jse.2006.08.001Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar have shown that expression levels of TNF-α, IL-1, and IL-6 are high in the joint capsule, in the subacromial bursa, and in joint fluid in patients with frozen shoulder. These data lend support to the hypothesis that indirect effects of viral infection may be involved in the development of AC. Lastly, it should be borne in mind that, in addition to the direct and indirect effects of SARS-CoV-2, viral infection may be related to the development of AC resulting from the marked changes in lifestyle induced by the pandemic, especially those due to quarantine. Indeed, we believe that a sedentary lifestyle is associated with a number of side effects, as is confirmed by extensive reports indicating that lack of physical activity results in and exacerbates musculoskeletal discomfort and pain.31Memari A. Shariat A. Anastasio A.T. Rising incidence of musculoskeletal discomfort in the wake of the COVID-19 crisis.Work. 2020; 66: 751-753https://doi.org/10.3233/WOR-203221Crossref PubMed Scopus (18) Google Scholar,38Shariat A. Cardoso J.R. Cleland J.A. Danaee M. Ansari N.N. Kargarfard M. et al.Prevalence rate of neck, shoulder and lower back pain in association with age, body mass index and gender among Malaysian office workers.Work. 2018; 60: 191-199https://doi.org/10.3233/WOR-2738Crossref PubMed Google Scholar The main limitations of our study are as follows: the limited size of the study group, although it should be borne in mind that we enrolled highly selected patients who had recently suffered from COVID-19 and who had AC of the shoulder with no other apparent causes; SARSCoV-2 was not specifically detected in the shoulder tissues of our patients, nor can we provide incontrovertible data supporting the correlation between overexpression of inflammatory mediators of COVID-19 and the development of AC of the shoulder; the lack of a short- and long-term evaluation of patients regarding the evolution and treatment of AC; the absence of a control group consisting of patients with AC that did not occur after COVID-19. Despite the possibility that there may be a correlation between COVID-19 and AC for the reasons we have provided, this case series cannot describe a cause-and-effect relationship. We present our series of 12 patients with AC of the shoulder that developed shortly after COVID-19. We hypothesize that AC may be related to the infectious disease and that both direct and indirect effects of SARS-CoV-2 infection may be involved in its development, as may the sedentary lifestyle forced on these patients by this disease.
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