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Smoking Predisposes to Rotator Cuff Pathology and Shoulder Dysfunction: A Systematic Review

      Purpose

      To investigate the association of smoking with rotator cuff (RTC) disease and shoulder dysfunction, defined as poor scores on shoulder rating scales.

      Methods

      A systematic review was performed using a search strategy based on “shoulder AND [smoke OR smoking OR nicotine OR tobacco].” English-language clinical or basic science studies testing the association of smoking and shoulder dysfunction on shoulder rating scales or disease of the soft tissue of the shoulder were included. Level V evidence studies and articles reporting only on surgery outcomes, subjective symptoms, adhesive capsulitis, or presence of fracture or oncologic mass were excluded.

      Results

      Thirteen studies were included, comprising a total of 16,172 patients, of whom 6,081 were smokers. All 4 clinical studies addressing the association between smoking and patient-reported shoulder symptoms and dysfunction in terms of poor scores on shoulder rating scales (i.e., Simple Shoulder Test; University of California, Los Angeles shoulder scale; and self-reported surveys) confirmed this correlation with 6,678 patients, of whom 1,723 were smokers. Two of four studies documenting provider-reported RTC disease comprised 8,461 patients, of whom 4,082 were smokers, and found a time- and dose-dependent relation of smoking with RTC tears and a correlation of smoking with impingement syndrome. Smoking was also reported in 4 other articles to be associated with the prevalence of larger RTC tears or tears with pronounced degenerative changes in 1,033 patients, of whom 276 were smokers, and may accelerate RTC degeneration, which could result in tears at a younger age. In addition, 1 basic science study showed that nicotine increased stiffness of the supraspinatus tendon in a rat model.

      Conclusions

      Smoking is associated with RTC tears, shoulder dysfunction, and shoulder symptoms. Smoking may also accelerate RTC degeneration and increase the prevalence of larger RTC tears. These correlations suggest that smoking may increase the risk of symptomatic RTC disease, which could consequently increase the need for surgical interventions.

      Level of Evidence

      Level IV, systematic review of Level II through IV studies.
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      References

        • Centers for Disease Control and Prevention
        Vital signs: Current cigarette smoking among adults aged ≥18 years—United States, 2005-2010.
        MMWR Morb Mortal Wkly Rep. 2011; 60: 1207-1212
        • Centers for Disease Control and Prevention
        Smoking-attributable mortality, years of potential life lost, and productivity losses—United States, 2000-2004.
        MMWR Morb Mortal Wkly Rep. 2008; 57: 1226-1228
        • Lee J.J.
        • Patel R.
        • Biermann J.S.
        • Dougherty P.J.
        The musculoskeletal effects of cigarette smoking.
        J Bone Joint Surg Am. 2013; 95: 850-859
        • Santiago-Torres J.
        • Flanigan D.C.
        • Butler R.B.
        • Bishop J.Y.
        The effect of smoking on rotator cuff and glenoid labrum surgery: A systematic review.
        Am J Sports Med. 2015; 43: 745-751
        • Tashjian R.Z.
        Epidemiology, natural history, and indications for treatment of rotator cuff tears.
        Clin Sports Med. 2012; 31: 589-604
        • Prasad N.
        • Odumala A.
        • Elias F.
        • Jenkins T.
        Outcome of open rotator cuff repair. An analysis of risk factors.
        Acta Orthop Belg. 2005; 71: 662-666
        • Milgrom C.
        • Schaffler M.
        • Gilbert S.
        • van Holsbeeck M.
        Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender.
        J Bone Joint Surg Br. 1995; 77: 296-298
        • Minagawa H.
        • Yamamoto N.
        • Abe H.
        • et al.
        Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: From mass-screening in one village.
        J Orthop. 2013; 10: 8-12
        • Moher D.
        • Liberati A.
        • Tetzlaff J.
        • Altman D.G.
        Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement.
        Int J Surg. 2010; 8: 336-341
        • Obremskey W.T.
        • Pappas N.
        • Attallah-Wasif E.
        • Tornetta III, P.
        • Bhandari M.
        Level of evidence in orthopaedic journals.
        J Bone Joint Surg Am. 2005; 87: 2632-2638
        • McRae S.
        • Leiter J.
        • Walmsley C.
        • Rehsia S.
        • Macdonald P.
        Relationship between self-reported shoulder function/quality of life, body mass index, and other contributing factors in patients awaiting rotator cuff repair surgery.
        J Shoulder Elbow Surg. 2011; 20: 57-61
        • Rechardt M.
        • Shiri R.
        • Karppinen J.
        • Jula A.
        • Heliovaara M.
        • Viikari-Juntura E.
        Lifestyle and metabolic factors in relation to shoulder pain and rotator cuff tendinitis: A population-based study.
        BMC Musculoskelet Disord. 2010; 11: 165
        • Kane S.
        • Conus S.
        • Haltom D.
        • Hirshorn K.
        • Pak Y.
        • Vigdorchik J.
        A shoulder health survey: Correlating behaviors and comorbidities with shoulder problems.
        Sports Health. 2010; 2: 119-134
        • Mallon W.J.
        • Misamore G.
        • Snead D.S.
        • Denton P.
        The impact of preoperative smoking habits on the results of rotator cuff repair.
        J Shoulder Elbow Surg. 2004; 13: 129-132
        • Baumgarten K.M.
        • Gerlach D.
        • Galatz L.M.
        • et al.
        Cigarette smoking increases the risk for rotator cuff tears.
        Clin Orthop Relat Res. 2010; 468: 1534-1541
        • Fehringer E.V.
        • Sun J.
        • VanOeveren L.S.
        • Keller B.K.
        • Matsen III, F.A.
        Full-thickness rotator cuff tear prevalence and correlation with function and co-morbidities in patients sixty-five years and older.
        J Shoulder Elbow Surg. 2008; 17: 881-885
        • Tangtrakulwanich B.
        • Kapkird A.
        Analyses of possible risk factors for subacromial impingement syndrome.
        World J Orthop. 2012; 3: 5-9
        • Titchener A.G.
        • White J.J.
        • Hinchliffe S.R.
        • Tambe A.A.
        • Hubbard R.B.
        • Clark D.I.
        Comorbidities in rotator cuff disease: A case-control study.
        J Shoulder Elbow Surg. 2014; 23: 1282-1288
        • Ichinose R.
        • Sano H.
        • Kishimoto K.N.
        • Sakamoto N.
        • Sato M.
        • Itoi E.
        Alteration of the material properties of the normal supraspinatus tendon by nicotine treatment in a rat model.
        Acta Orthop. 2010; 81: 634-638
        • Carbone S.
        • Gumina S.
        • Arceri V.
        • Campagna V.
        • Fagnani C.
        • Postacchini F.
        The impact of preoperative smoking habit on rotator cuff tear: Cigarette smoking influences rotator cuff tear sizes.
        J Shoulder Elbow Surg. 2012; 21: 56-60
        • Kane S.M.
        • Dave A.
        • Haque A.
        • Langston K.
        The incidence of rotator cuff disease in smoking and non-smoking patients: A cadaveric study.
        Orthopedics. 2006; 29: 363-366
        • Kukkonen J.
        • Kauko T.
        • Virolainen P.
        • Aarimaa V.
        Smoking and operative treatment of rotator cuff tear.
        Scand J Med Sci Sports. 2014; 24: 400-403
        • Lundgreen K.
        • Lian O.B.
        • Scott A.
        • Nassab P.
        • Fearon A.
        • Engebretsen L.
        Rotator cuff tear degeneration and cell apoptosis in smokers versus nonsmokers.
        Arthroscopy. 2014; 30: 936-941
        • Snyder S.J.
        Arthroscopic classification of rotator cuff lesions and surgical decision making.
        in: Shoulder arthroscopy. Ed 2. Lippincott Williams & Wilkins, Philadelphia2003: 201-207
        • Rothman S.M.
        • Huang Z.
        • Lee K.E.
        • Weisshaar C.L.
        • Winkelstein B.A.
        Cytokine mRNA expression in painful radiculopathy.
        J Pain. 2009; 10: 90-99
        • Binshtok A.M.
        • Wang H.
        • Zimmermann K.
        • et al.
        Nociceptors are interleukin-1beta sensors.
        J Neurosci. 2008; 28: 14062-14073
        • Eliav E.
        • Benoliel R.
        • Herzberg U.
        • Kalladka M.
        • Tal M.
        The role of IL-6 and IL-1beta in painful perineural inflammatory neuritis.
        Brain Behav Immun. 2009; 23: 474-484
        • Blaine T.A.
        • Kim Y.S.
        • Voloshin I.
        • et al.
        The molecular pathophysiology of subacromial bursitis in rotator cuff disease.
        J Shoulder Elbow Surg. 2005; 14: 84S-89S
        • Gotoh M.
        • Hamada K.
        • Yamakawa H.
        • et al.
        Interleukin-1-induced glenohumeral synovitis and shoulder pain in rotator cuff diseases.
        J Orthop Res. 2002; 20: 1365-1371
        • Gotoh M.
        • Hamada K.
        • Yamakawa H.
        • et al.
        Interleukin-1-induced subacromial synovitis and shoulder pain in rotator cuff diseases.
        Rheumatology (Oxford). 2001; 40: 995-1001
        • Ko J.Y.
        • Wang F.S.
        • Huang H.Y.
        • Wang C.J.
        • Tseng S.L.
        • Hsu C.
        Increased IL-1beta expression and myofibroblast recruitment in subacromial bursa is associated with rotator cuff lesions with shoulder stiffness.
        J Orthop Res. 2008; 26: 1090-1097
        • Nakama K.
        • Gotoh M.
        • Yamada T.
        • et al.
        Interleukin-6-induced activation of signal transducer and activator of transcription-3 in ruptured rotator cuff tendon.
        J Int Med Res. 2006; 34: 624-631
        • Voloshin I.
        • Gelinas J.
        • Maloney M.D.
        • O'Keefe R.J.
        • Bigliani L.U.
        • Blaine T.A.
        Proinflammatory cytokines and metalloproteases are expressed in the subacromial bursa in patients with rotator cuff disease.
        Arthroscopy. 2015; 21 (Available at www.arthroscopyjournal.org): 1076.e1-1076.e9
        • Karas V.
        • Hussey K.
        • Romeo A.R.
        • Verma N.
        • Cole B.J.
        • Mather III, R.C.
        Comparison of subjective and objective outcomes after rotator cuff repair.
        Arthroscopy. 2013; 29: 1755-1761
        • Teefey S.A.
        • Hasan S.A.
        • Middleton W.D.
        • Patel M.
        • Wright R.W.
        • Yamaguchi K.
        Ultrasonography of the rotator cuff. A comparison of ultrasonographic and arthroscopic findings in one hundred consecutive cases.
        J Bone Joint Surg Am. 2000; 82: 498-504
        • Zumstein M.A.
        • Jost B.
        • Hempel J.
        • Hodler J.
        • Gerber C.
        The clinical and structural long-term results of open repair of massive tears of the rotator cuff.
        J Bone Joint Surg Am. 2008; 90: 2423-2431
        • Rhee Y.G.
        • Cho N.S.
        • Yoo J.H.
        Clinical outcome and repair integrity after rotator cuff repair in patients older than 70 years versus patients younger than 70 years.
        Arthroscopy. 2014; 30: 546-554
        • Charousset C.
        • Bellaiche L.
        • Kalra K.
        • Petrover D.
        Arthroscopic repair of full-thickness rotator cuff tears: Is there tendon healing in patients aged 65 years or older?.
        Arthroscopy. 2010; 26: 302-309
        • McElvany M.D.
        • McGoldrick E.
        • Gee A.O.
        • Neradilek M.B.
        • Matsen III, F.A.
        Rotator cuff repair: Published evidence on factors associated with repair integrity and clinical outcome.
        Am J Sports Med. 2015; 43: 491-500
        • Oh J.H.
        • Kim S.H.
        • Ji H.M.
        • Jo K.H.
        • Bin S.W.
        • Gong H.S.
        Prognostic factors affecting anatomic outcome of rotator cuff repair and correlation with functional outcome.
        Arthroscopy. 2009; 25: 30-39
        • Lafosse L.
        • Brozska R.
        • Toussaint B.
        • Gobezie R.
        The outcome and structural integrity of arthroscopic rotator cuff repair with use of the double-row suture anchor technique.
        J Bone Joint Surg Am. 2007; 89: 1533-1541
        • Katzer A.
        • Wening J.V.
        • Becker-Mannich H.U.
        • Lorke D.E.
        • Jungbluth K.H.
        Rotator cuff rupture. Vascular supply and collagen fiber processes as pathogenetic factors.
        Unfallchirurgie. 1997; 23 ([in German]): 52-59
        • Determe D.
        • Rongieres M.
        • Kany J.
        • et al.
        Anatomic study of the tendinous rotator cuff of the shoulder.
        Surg Radiol Anat. 1996; 18: 195-200
        • Ling S.C.
        • Chen C.F.
        • Wan R.X.
        A study on the vascular supply of the supraspinatus tendon.
        Surg Radiol Anat. 1990; 12: 161-165
        • Itoi E.
        • Berglund L.J.
        • Grabowski J.J.
        • et al.
        Tensile properties of the supraspinatus tendon.
        J Orthop Res. 1995; 13: 578-584
        • Matsen III, F.A.
        • Titelman R.M.
        • Lippitt S.B.
        • Rockwood Jr., C.A.
        Rotator cuff.
        in: Rockwood Jr., C.A. Matsen III, F.A. Wirth M.A. Lippitt S.B. The shoulder. Ed 3. WB Saunders, Philadelphia2004: 795-878
        • Tuite M.J.
        • Turnbull J.R.
        • Orwin J.F.
        Anterior versus posterior, and rim-rent rotator cuff tears: Prevalence and MR sensitivity.
        Skeletal Radiol. 1998; 27: 237-243