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Smoking Predisposes to Rotator Cuff Pathology and Shoulder Dysfunction: A Systematic Review
Systematic Review
Smoking Predisposes to Rotator Cuff Pathology and Shoulder Dysfunction: A Systematic Review Julie Y. Bishop, M.D., Juan E. Santiago-Torres, M.S., Nathan Rimmke, M.D., and David C. Flanigan, M.D.
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.
T
he prevalence of smoking remains close to 20% in the general population, being highest in persons below the poverty level or aged 22 to 44 years.1 Smoking has been strongly linked to cancer, chronic obstructive pulmonary disease, and cardiovascular disease.2 Smoking has also been shown to have adverse clinical musculoskeletal effects, including an increased risk of sustaining a fracture, nonunion and delayed union of fractures, and decreased bone mineral density.3 In addition, we recently showed in a systematic From the Department of Orthopaedics, The Ohio State University, Columbus, Ohio, U.S.A. The authors report the following potential conflict of interest or source of funding: D.C.F. receives support from Sanofi and Smith & Nephew. Received October 28, 2014; accepted January 21, 2015. Address correspondence to Julie Y. Bishop, M.D., Sports Medicine Center, The Ohio State University, 2050 Kenny Rd, Ste 3100, Columbus, OH 43221, U.S.A. E-mail: [email protected] Ó 2015 by the Arthroscopy Association of North America 0749-8063/14903/$36.00 http://dx.doi.org/10.1016/j.arthro.2015.01.026
review that smoking is associated with poor clinical outcomes after rotator cuff (RTC) repair and poor healing outcomes of small to medium tears.4 Because smoking temporarily decreases tissue oxygenation and nicotine is a potent vasoconstrictor, the effect of smoking may be marked in already hypovascular areas, such as the soft tissue within the shoulder.5 Hence it is reasonable to assume that smoking is associated with RTC pathology. Although individual studies have been published on the effects of smoking on normal shoulder tendon tissue, to date, there have been no comprehensive reviews of the literature on the topic. With the increasing life expectancy and as the baby boomer generation ages, orthopaedic surgeons are seeing more elderly patients presenting with degenerative RTC tears.6 Some studies suggest that the prevalence and extent of degenerative RTC tears increase with advancing age,7,8 highlighting the importance of addressing risk factors to prevent RTC tears. Therefore the purpose of this study was to investigate the
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association of smoking with RTC disease and shoulder dysfunction. We hypothesized that smoking has a negative effect on shoulder health.
Methods A systematic review was conducted according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines9 (Fig 1). The search strategy was based on “shoulder AND [smoke OR smoking OR nicotine OR tobacco].” The search was independently confirmed by the coauthors (J.Y.B., J.E.S-T., N.R., D.C.F.) on October 4, 2014. The following medical databases were used: PubMed, CINAHL (Cumulative Index to Nursing and Allied Health Literature), SPORTDiscus, and The Cochrane Library. We included studies with Levels I, II, III, and IV evidence as defined by the Oxford Centre for EvidenceBased Medicine and used by the American version of The Journal of Bone and Joint Surgery.10 Meeting and conference abstracts were not eligible for inclusion. The senior author (J.Y.B.) made the final decision on article inclusion if there was disagreement among authors. Top hits in Web search engines and all references within included studies were checked to identify potentially relevant studies missed by the initial database search. Any English-language clinical articles studying smoking and shoulder function assessed with shoulder rating scales or RTC or glenoid labrum disease with evidence Levels I through IV were included. Basic science studies analyzing the anatomy, histology, pathology, biomechanics, or imaging characteristics associated with RTC or glenoid labrum disorders were also included. The exclusion criteria consisted of noneEnglishlanguage studies and studies of Level V evidence (i.e., single-case report, expert opinion, or personal observation). Any clinical and basic science studies analyzing any joint other than the shoulder were also excluded. In addition, studies reporting only subjective pain findings or on adhesive capsulitis were excluded. Finally, studies reporting on fractures or oncologic masses around the shoulder were excluded, as were studies analyzing only the outcomes of surgery, without reporting preoperative status. Continuous variable data were reported as means and standard deviations from the means. Categorical variable data were reported as frequencies with percentages. Associations were reported as odds ratios (ORs) with corresponding 95% confidence intervals (CIs). P < .05 was considered significant.
Results Thirteen studies were identified for inclusion and analysis, comprising 16,172 patients, of whom 6,081 were smokers. Four of these studies were clinical
Fig 1. Search strategy according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines. Thirteen studies were identified for inclusion. No studies on smoking and glenoid labrum disease were found. (RTC, rotator cuff.)
studies that addressed the association between smoking and patient-reported shoulder dysfunction (i.e., poor scores on shoulder rating scales) and symptoms (Table 1). Another 4 clinical studies examined the correlation between smoking and provider-reported RTC disease (Table 2). The other studies investigated the relation of smoking and degree of RTC pathology or mechanical properties of the RTC (3 clinical, 1 cadaveric, and 1 basic science study) (Table 3). No studies specifically exploring the effects of smoking on the glenoid labrum were found. Patient-Reported Shoulder Symptoms and Dysfunction Smokers were more likely to report shoulder pain and decreased shoulder function (Table 1). With a total of 6,678 patients (mean age, 52 years), of whom 1,723 were smokers, all 4 clinical studies reviewed found a significant negative association between smoking and shoulder function and symptoms. McRae et al.11 performed a retrospective cohort study, which included 54 patients who underwent arthroscopic RTC repair, only 9 of whom were smokers. They found that smoking status was negatively correlated with preoperative Simple Shoulder Test scores (P ¼ .003). However, smoking status was not associated
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Table 1. Clinical Studies on Smoking and Patient-Reported Symptoms and Shoulder Dysfunction Journal J Shoulder Elbow Surg
No. of Patients (Mean Age, yr) 54 (58.2)
BMC Musculoskelet Disorders
6,237 (51.9)
Sports Health
163
Authors McRae et al.11 (2011)
Rechardt et al.12 (2010)
Kane et al.13 (2010)
Mallon et al.14 (2004)
J Shoulder Elbow Surg
224 (52.3)
Pertinent Findings Smoking was associated with poor shoulder function and pain scores. Smoking was correlated with SST scores (P ¼ .003) and had a greater correlation when combined with female sex and work-related injury (P < .001). However, there was no correlation with ASES scores (P ¼ .184). Patients with unilateral shoulder pain (OR, 1.9; 95% CI, 1.3 to 2.9) and bilateral shoulder pain (OR, 1.8; 95% CI, 1.0 to 3.1) were more likely to be currently smoking men who had smoked for >20 pack-years and women who had smoked for 10 to 20 packyears, respectively. Smoking was not associated with chronic RTC tendinitis. Shoulder pain and loss of function were found to be proportional to smoking. Smokers had worse mean scores on the Subjective Shoulder Rating System assessment (P ¼ .005), Shoulder Rating Questionnaire (P ¼ .0008), and Oxford Shoulder Questionnaire (P ¼ .0042). Smokers also reported lower active range of motion in both the left and right shoulders (P ¼ .024). No significant difference was found between smokers of <1 pack per day and smokers of 1 pack per day. Preoperative scores showed that smokers had higher pain scores (P < .0001) and lower UCLA scores (P ¼ .00025) than nonsmokers.
ASES, American Shoulder and Elbow Surgeons; CI, confidence interval; OR, odds ratio; RTC, rotator cuff; SST, Simple Shoulder Test; UCLA, University of California, Los Angeles shoulder scale.
with worse preoperative American Shoulder and Elbow Surgeons scores (P ¼ .184). Rechardt et al.12 interviewed and examined 6,237 patients, of whom 1,589 were smokers, to correlate
smoking and shoulder pain. This cross-sectional study found that current smoking status was associated with unilateral shoulder pain in men but not in women. The authors found that currently smoking men who had a
Table 2. Clinical Studies on Smoking and Provider-Reported Rotator Cuff Disease Authors Baumgarten et al.15 (2010)
Fehringer et al.16 (2008)
Tangtrakulwanich and Kapbird17 (2012)
Titchener et al.18 (2014)
Journal Clin Orthop Relat Res
J Shoulder Elbow Surg
World J Orthop
J Shoulder Elbow Surg
CI, confidence interval; OR, odds ratio; RTC, rotator cuff.
No. of Patients (Mean Age, yr) 584 (57.7)
104 (71.4)
302 (50)
7,471 (55)
Pertinent Findings This study showed a time- and dose-dependent relation between smoking and RTC tears. The correlation increased when smoking occurred within 10 yr of presentation (OR, 4.24; CI, 1.75 to 10.25; P ¼ .0006) and was significant in patients with a history of smoking 1 to 2 packs per day (OR, 1.66; P ¼ .009) and even greater for 2 packs per day (OR, 3.35; P ¼ .0007). Ultrasonography was used to diagnose RTC tears. No statistically significant association of smoking with increasing RTC tear prevalence was found (P ¼ .52) in 200 shoulders from 104 patients aged 65 yr. Ultrasonography was used to diagnose RTC tears. Current smokers were at greater risk of impingement syndrome compared with nonsmokers (OR, 6.8; 95% CI, 1.2 to 39). Impingement syndrome was diagnosed with a lidocaine subacromial injection test. Current smoking status was not associated with a diagnosis of RTC disease (OR, 1.03; CI, 0.91 to 1.15), whereas a history of smoking was associated with RTC disease (OR, 1.24; CI, 1.10 to 1.39). This effect disappeared after adjustment for number of general practice consultation rate per year (OR, 1.09; CI, 0.96 to 1.23).
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Table 3. Studies on Smoking and Degree of Rotator Cuff Pathology
Journal
Type of Study or No. of Patients (Mean Age, yr)
Pertinent Findings
Animal model (rat)
Nicotine caused an increase in the calculated elastic modulus of the supraspinatus tendon (P < .05).
Authors Basic science study Ichinose et al.19 (2010)
Acta Orthop
Clinical studies Carbone et al.20 (2012)
J Shoulder Elbow Surg
Kane et al.21 (2006)
Orthopedics
Cadaveric study, 36 (75)
Kukkonen et al.22 (2014)
Scand J Med Sci Sports
564 (59.8)
Lundgreen et al.23 (2014)
Arthroscopy
25 (55.6)
408 (59)
The analysis resulted in a finding suggestive of significance of an increase in the severity of RTC tears as the average number of cigarettes smoked increased (P ¼ .099). When combining type II, III, and IV tears (SCOI classification), the authors showed that increasing tear severity was associated with increasing daily numbers of cigarettes (P ¼ .04). In addition, the total number of cigarettes smoked over a lifetime differed significantly between patients with a small tear and those with at least a type II tear (P ¼ .032). Macroscopic RTC tears were more likely in cadavers with a history of smoking, and the presence of advanced microscopic RTC pathology was more than twice as likely in cadavers with a history of smoking. The data were not statistically significant. Smokers were significantly younger, with equally large tears, compared with nonsmokers (P < .001). There was no significant difference in preoperative Constant score (P ¼ .075) or mean size of intraoperatively measured tendon tear (P ¼ .5) in smokers v nonsmokers. Samples of the supraspinatus muscle were obtained arthroscopically in patients undergoing surgery for full-thickness RTC tears. Those with a smoking history of at least half a pack per day had a longer duration of symptoms (19 months v 11 months, P < .05), were younger (52 yr [SD, 6.4 yr] v 58 yr [SE, 5.8 yr]; P < .01), and had more advanced degeneration with a higher Bonar score (13.5 v 9, P < .001) than nonsmokers. The study also showed increased density of apoptotic cells (P < .024), reduced tenocyte density (P < .019), and upregulation of proliferative activity (P < .0001) in tendons of patients with a smoking history.
RTC, rotator cuff; SCOI, Southern California Orthopedic Institute.
history of smoking of more than 20 pack-years were at the highest risk of unilateral shoulder pain (OR, 1.9; 95% CI, 1.3 to 2.9). Currently smoking women who had a history of smoking of 10 to 20 pack-years were at highest risk of bilateral shoulder pain (OR, 1.8; 95% CI, 1.0 to 3.1). Smoking was not found to be associated with the presence of chronic RTC tendinitis. Self-reported shoulder surveys have also found a correlation between smoking and shoulder dysfunction. Kane et al.13 provided a subjective assessment of shoulder function using 3 different patient-response surveys, answered by 163 patients. The Oxford Shoulder Questionnaire (P ¼ .0042), the Shoulder Rating Questionnaire (P ¼ .0008), and the Subjective Shoulder Rating System (P ¼ .005) all found smokers (n ¼ 30) to have worse shoulder function than nonsmokers (n ¼ 133). In addition, smokers reported higher complaints of pain (P ¼ .04) and lower active range of motion (P ¼ .024). In addition, smoking status has been shown to have a negative effect on patients with RTC tendon tears. Mallon et al.14 studied 224 patients and reported that
smokers (n ¼ 95) had higher preoperative pain scores (P < .0001) and lower preoperative University of California, Los Angeles scores (P ¼ .00025) than nonsmokers (n ¼ 129). Provider-Reported RTC Disease Mixed results were found in the 4 clinical studies reviewed on smoking and provider-reported RTC disease, comprising 8,461 patients, of whom 4,082 were smokers (Table 2). Two of these studies used ultrasonography to assess the prevalence of RTC tears. Baumgarten et al.15 found a dose-dependent and time-dependent relation between smoking and RTC tears. They analyzed 584 patients, of whom 473 were smokers, who underwent a diagnostic shoulder ultrasound for unilateral, atraumatic shoulder pain with no history of shoulder surgery. They reported RTC tears to be more prevalent in patients with a history of smoking (P ¼ .002) and in those with a history of smoking within 10 years of presentation (P ¼ .0006). They also found that the RTC tear cohort had a higher rate of tobacco use in terms of the mean number of packs per day (P ¼ .004), a
SMOKING AND SHOULDER HEALTH
longer duration of smoking (P ¼ .05), and a larger tobacco exposure (P ¼ .0006). Fehringer et al.16 also used ultrasonography to determine the prevalence of RTC tears and found contrasting results to those of Baumgarten et al. No statistically significant association of smoking with increasing RTC tear prevalence was found in 200 shoulders of 104 patients aged 65 years or older, of whom 78 had a smoking history (P ¼ .52). Tangtrakulwanich and Kapbird17 performed a casecontrol study that evaluated the association between smoking and impingement syndrome in 302 patients. Patients who currently smoked (n ¼ 26) had a 6.8 times greater risk of impingement syndrome than nonsmokers (OR, 6.8; 95% CI, 1.2 to 39). Impingement syndrome was diagnosed with a lidocaine subacromial injection test. In a large case-control study, Titchener et al.18 looked at 5,000 patients with RTC disease and 5,000 controls. Smoking data were available for 78.9% of cases and 70.5% of controls, for a total of 7,471 patients, of whom 3,505 had a smoking history. Current smoking status (n ¼ 1,761) was not associated with a diagnosis of RTC disease (OR, 1.03; 95% CI, 0.91 to 1.15). A history of smoking (n ¼ 1,744) was associated with RTC disease (OR, 1.24; 95% CI, 1.1 to 1.39), although this effect disappeared after adjustment for yearly rate of number of patient visits to a general practitioner (OR, 1.09; 95% CI, 0.96 to 1.23). Mechanical Properties and Degree of RTC Pathology The literature has also shown a link between smoking and the degree of RTC pathology. Four of five studies reviewed on this topic found a statistically significant correlation between the two (Table 3). Ichinose et al.19 performed a basic science study in which they randomized 27 rats to 3 groups. Over a 12week period, a subcutaneously implanted osmotic pump delivered either a high-dose nicotine solution (45 ng/mL), a low-dose nicotine solution (22.5 ng/mL), or saline solution (controls). The authors found that the elastic modulus of the supraspinatus tendon in the high- and low-dose groups was higher than that in the control group (P ¼ .04 and P ¼ .03, respectively). A higher elastic modulus in a tendon indicates that it is stiffer and more susceptible to injury. Carbone et al.20 found a correlation among cigarette smoking, presence of RTC tears, and RTC tear size. Their study comprised 408 patients, of whom 131 were smokers, who underwent arthroscopic RTC repair. The RTC tears were classified intraoperatively according to the Southern California Orthopedic Institute classification system24: type I tears are small, complete tears, such as a puncture wound; type II tears are moderate tears (<2 cm) that encompass only 1 tendon, with no retraction of the tendon ends; type III tears are large (3
5
to 4 cm), with minimal retraction of the torn edge; and type IV tears are massive tears, involving 2 or more tendons and associated with retraction and scarring, and are frequently irreparable. Carbone et al. showed that the frequency of smokers was 23.2% among patients with a small full-thickness tear in contrast to 34.8% among those with a larger full-thickness tear (P ¼ .033). When combining type II, III, and IV tears, they found an increasing severity of tears associated with an increasing daily number of cigarettes (P ¼ .04). In addition, the total number of lifetime cigarettes smoked was significantly higher in patients with at least a type II tear (P ¼ .032). Kukkonen et al.22 looked at preoperative data for 564 consecutive shoulders undergoing arthroscopic repair for RTC tears. They found a statistically significant difference in the mean age of smokers (55 years; SD, 9.1 years; n ¼ 114) compared with nonsmokers (61 years; SD, 9.4 years; n ¼ 450) at the time of surgery (P < .001). There was no difference in the size of the tear between groups. Although the pack-years of smoking did not statistically correlate with preoperative Constant scores (P ¼ .075), the data suggest that smoking is a risk factor for tears at a younger age. Kane et al.21 did not find a statistically significant correlation between the incidence of RTC disease and smoking, although there was a strong trend toward such a finding. They dissected 72 shoulders in 36 cadavers to identify microscopic and macroscopic evidence of RTC disease. They also looked at microscopic samples of lung tissue from each cadaver to determine smoking history, identifying 21 of the cadavers as smokers. Of the 72 shoulders, 36 had evidence of macroscopic RTC disease (full- or partial-thickness RTC tear on gross visualization), and 23 of these had evidence of a smoking history compared with only 13 that had no evidence of a smoking history. Microscopic evidence of RTC disease (grade 3 or 4 fibrous degeneration) was more than twice as likely in cadavers with evidence of a smoking history. Again, although there were strong trends, none of these data were statistically significant. Lundgreen et al.23 found a statistically significant association of smoking with symptoms, tear at a younger age, and worsened histopathology of the supraspinatus tendon in 25 patients, of whom 10 were smokers. Samples of the supraspinatus muscle were obtained arthroscopically in patients undergoing arthroscopic surgery for full-thickness RTC tears. Those with a smoking history of at least half a pack per day were found to have a longer duration of symptoms (19 months v 11 months, P < .05) and had more advanced degeneration with a higher Bonar score (13.5 v 9, P < .001) than nonsmokers. In addition, the patients with a smoking history were younger than the nonsmokers (52 years [SD, 6.4 years] v 58 years [SE,
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5.8 years]; P < .01). Lundgreen et al. also showed increased density of apoptotic cells (P < .024), reduced tenocyte density (P < .019), and upregulation of proliferative activity (P < .0001) in tendons of patients with a smoking history.
Discussion Our systematic review confirmed that smoking has a negative influence on the health of the shoulder. Specifically, we report that smoking is associated with a higher prevalence of symptomatic shoulder disease and dysfunction (i.e., poor scores on shoulder rating scales), risk of RTC degeneration, and larger RTC tears, as well as an increased risk of tears at a younger age. The current literature shows mixed results regarding whether smokers have a higher overall prevalence of RTC tendon tears. This study found that smokers have higher amounts of shoulder pain and worse shoulder function than nonsmokers as assessed with the Shoulder Simple Test; University of California, Los Angeles shoulder scale; and self-reported shoulder surveys. Smoking increases the number of circulating proinflammatory cytokines, and this may prolong inflammation and increase sensitivity to pain.25-27 Shoulder diseases, such as RTC lesions and subacromial bursitis, have been associated with increased expression of these cytokines.28-33 These findings suggest that smoking could lead to an increased need for treatment because it increases the risk of symptomatic shoulder disease. Determining what kind of treatment is necessary is difficult because we do not have any controlled data regarding how well smokers respond to nonoperative management of RTC disease. In addition, Mallon et al.14 showed that smoking status has negative effects on patients with proven RTC tears. Thus this finding further reinforces the idea that smokers are less likely to cope and undergo successful nonoperative treatment. This is a major clinical concern for shoulder surgeons because it has been proved in the literature that smoking leads to poor clinical and healing outcomes of RTC repair.4 In addition, some studies have shown that the patients who benefit most from arthroscopic RTC repair have good preoperative strength.34 If we use preoperative functional status as a predictor of surgical outcome, smokers will have worse surgical outcomes. The literature is less clear on how smoking affects the prevalence of RTC disease. Baumgarten et al.,15 Carbone et al.,20 and Tangtrakulwanich and Kapbird17 did show an association between smoking and the prevalence of RTC tears and impingement syndrome, whereas Fehringer et al.,16 Titchener et al.,18 and Kane et al.21 did not. Baumgarten et al. and Fehringer et al. both used ultrasonography to detect the prevalence of RTC tears. Ultrasound has been shown to be 96% accurate, 100% sensitive, and 85% specific for diagnosing
full-thickness RTC tears.35 However, the sensitivity drops to 67%, with the specificity remaining at 85%, when diagnosing partial-thickness RTC tears. This may decrease the validity of the results of Baumgarten et al. and Fehringer et al. Titchener et al. used a database to identify patients with a diagnosis code related to RTC disease. They did not specify how they determined the diagnosis, and thus we cannot comment on the accuracy of their results. The gold standard to identify the presence of an RTC tear is either diagnostic arthroscopy or open dissection, and only 2 studies included in our literature review used these diagnostic modalities. Carbone et al. used arthroscopy to show that smokers do have a higher prevalence of RTC tears. In addition, Kane et al. showed a strong trend linking smoking and RTC disease through cadaveric dissections, although their data did not reach statistical significance likely because not enough cadavers were included in the study and, hence, the power was insufficient. Carbone et al.,20 Kukkonen et al.,22 Kane et al.,21 and Lundgreen et al.23 showed a link between smoking and increasing degree of RTC pathology. Their studies confirmed that smokers have larger tears, higher grades of fibrous degeneration, and increased numbers of tears at a younger age. These findings are of clinical importance because larger RTC tears have a more unfavorable treatment history. This is because RTC tears are associated with higher retear rates than smaller tears after repair.36-38 Furthermore, smoking has been shown to decrease cuff healing4; thus smokers with larger tears are at an additional disadvantage regarding healing of the repair. Although many unhealed RTC repairs have been found to be clinically asymptomatic,39,40 one could surmise from the data presented in our review that smokers tend to have more RTC-related pain and perhaps would have more symptomatic unhealed RTC repairs. In addition, postoperative strength and function are worse after repair of large and massive RTC tears as compared with small tears.41 These findings should prompt the surgeon to take smoking status into consideration when assessing the prognosis for a patient undergoing an RTC repair procedure. The results discussed in this report are biologically plausible because vascular insufficiency to the critical portions of the shoulder are implicated in the genesis of RTC tears.42 Anatomic and histologic studies have confirmed a region of relative hypovascularity within the tendons of the supraspinatus and infraspinatus just proximal to their insertion on the greater tuberosity.42-44 Tobacco smoking likely contributes to the tendon degeneration processes because nicotine causes hypoxia, limiting blood supply to the hypovascular portion of the RTC.42 This hypoxic environment may lead to altered metabolism and a decreased healing response. In fact, Lundgreen et al.23 found increased density of apoptotic cells and reduced density of tenocytes in torn RTCs of
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patients with a smoking history. Another factor that could lead to pathologic processes in the shoulder is that smoking can change the mechanical properties of the RTC tendon. Ichinose et al.19 showed that tendons exposed to nicotine had a higher elastic modulus than controls. It has been previously shown that RTC tears commonly start at the anterior third of the supraspinatus tendon, where the elastic modulus is the highest.45-47 The aforementioned finding suggests that smoking increases the likelihood of an RTC tear by increasing the elastic modulus of the tendon. Ichinose et al. speculated that nicotine may increase the stiffness of the tendon through increased synthesis of collagen and reduced production of matrix metalloproteinase. No basic science studies were found that explored the effects of other toxins in cigarette smoke on the soft tissue of the shoulder. Therefore further study would potentially elucidate the causative components of tobacco smoke and the biochemical and pathophysiologic mechanisms in the setting of RTC pathology, which are essential in understanding whether nicotine replacement therapy is a viable option for patients at risk of RTC pathology. Limitations This systematic review has some limitations to consider. The literature meeting the inclusion criteria were only retrospective studies. Recall bias from patients perceiving smoking as the cause of their illness could have a significant impact on our results; hence prospectively designed studies could be of benefit. Studies performed in the hospital setting could result in selection bias toward patients with poor health, and those recruiting only from referral centers do not provide a true cross section of the population. Moreover, the use of only 1 ultrasonographer in some studies and differences between interviewers could result in observation bias. Some potential confounders are occupation and activity level, whereas age was controlled for in all the studies. In addition, a source of selection bias is inherent because only English-language studies were included. This review examined only tobacco smoking, not smokeless tobacco or nicotine patches or gum. In this study we did not control for the clinical measurements used, different criteria for inclusion as a smoker, and method for assessing RTC disease. Only 2 studies assessed tears intraoperatively, and 2 other studies used ultrasound, which has a high sensitivity and specificity for fullthickness tears but a lower sensitivity for partialthickness tears.35 None of the studies included were performed in developing countries. As a consequence of these limitations, it is challenging to draw generalizable conclusions from the studies.
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.
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15. Baumgarten KM, Gerlach D, Galatz LM, et al. Cigarette smoking increases the risk for rotator cuff tears. Clin Orthop Relat Res 2010;468:1534-1541. 16. Fehringer EV, Sun J, VanOeveren LS, Keller BK, Matsen FA III. 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. 17. Tangtrakulwanich B, Kapkird A. Analyses of possible risk factors for subacromial impingement syndrome. World J Orthop 2012;3:5-9. 18. Titchener AG, White JJ, Hinchliffe SR, Tambe AA, Hubbard RB, Clark DI. Comorbidities in rotator cuff disease: A case-control study. J Shoulder Elbow Surg 2014;23: 1282-1288. 19. Ichinose R, Sano H, Kishimoto KN, 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. 20. 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. 21. Kane SM, 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. 22. 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. 23. Lundgreen K, Lian OB, Scott A, Nassab P, Fearon A, Engebretsen L. Rotator cuff tear degeneration and cell apoptosis in smokers versus nonsmokers. Arthroscopy 2014;30:936-941. 24. Snyder SJ. Arthroscopic classification of rotator cuff lesions and surgical decision making. In: Shoulder arthroscopy. Ed 2. Philadelphia: Lippincott Williams & Wilkins, 2003;201-207. 25. Rothman SM, Huang Z, Lee KE, Weisshaar CL, Winkelstein BA. Cytokine mRNA expression in painful radiculopathy. J Pain 2009;10:90-99. 26. Binshtok AM, Wang H, Zimmermann K, et al. Nociceptors are interleukin-1beta sensors. J Neurosci 2008;28: 14062-14073. 27. 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. 28. Blaine TA, Kim YS, Voloshin I, et al. The molecular pathophysiology of subacromial bursitis in rotator cuff disease. J Shoulder Elbow Surg 2005;14:84S-89S. 29. Gotoh M, Hamada K, Yamakawa H, et al. Interleukin-1induced glenohumeral synovitis and shoulder pain in rotator cuff diseases. J Orthop Res 2002;20:1365-1371. 30. Gotoh M, Hamada K, Yamakawa H, et al. Interleukin-1induced subacromial synovitis and shoulder pain in rotator cuff diseases. Rheumatology (Oxford) 2001;40: 995-1001. 31. Ko JY, Wang FS, Huang HY, Wang CJ, Tseng SL, 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.
32. Nakama K, Gotoh M, Yamada T, et al. Interleukin-6induced activation of signal transducer and activator of transcription-3 in ruptured rotator cuff tendon. J Int Med Res 2006;34:624-631. 33. Voloshin I, Gelinas J, Maloney MD, O’Keefe RJ, Bigliani LU, Blaine TA. Proinflammatory cytokines and metalloproteases are expressed in the subacromial bursa in patients with rotator cuff disease. Arthroscopy 2015;21:1076.e1-1076.e9. Available at www.arthroscopyjournal.org. 34. Karas V, Hussey K, Romeo AR, Verma N, Cole BJ, Mather RC III. Comparison of subjective and objective outcomes after rotator cuff repair. Arthroscopy 2013;29: 1755-1761. 35. Teefey SA, Hasan SA, Middleton WD, Patel M, Wright RW, 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. 36. Zumstein MA, 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. 37. Rhee YG, Cho NS, Yoo JH. 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. 38. 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. 39. McElvany MD, McGoldrick E, Gee AO, Neradilek MB, Matsen FA III. Rotator cuff repair: Published evidence on factors associated with repair integrity and clinical outcome. Am J Sports Med 2015;43:491-500. 40. Oh JH, Kim SH, Ji HM, Jo KH, Bin SW, Gong HS. Prognostic factors affecting anatomic outcome of rotator cuff repair and correlation with functional outcome. Arthroscopy 2009;25:30-39. 41. 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. 42. Katzer A, Wening JV, Becker-Mannich HU, Lorke DE, Jungbluth KH. Rotator cuff rupture. Vascular supply and collagen fiber processes as pathogenetic factors. Unfallchirurgie 1997;23:52-59 [in German]. 43. 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. 44. Ling SC, Chen CF, Wan RX. A study on the vascular supply of the supraspinatus tendon. Surg Radiol Anat 1990;12:161-165. 45. Itoi E, Berglund LJ, Grabowski JJ, et al. Tensile properties of the supraspinatus tendon. J Orthop Res 1995;13:578-584. 46. Matsen FA III, Titelman RM, Lippitt SB, Rockwood CA Jr. Rotator cuff. In: Rockwood CA Jr, Matsen FA III, Wirth MA, Lippitt SB, eds. The shoulder. Ed 3. Philadelphia: WB Saunders, 2004;795-878. 47. Tuite MJ, Turnbull JR, Orwin JF. Anterior versus posterior, and rim-rent rotator cuff tears: Prevalence and MR sensitivity. Skeletal Radiol 1998;27:237-243.
Smoking Predisposes to Rotator Cuff Pathology and Shoulder Dysfunction: A Systematic Review Julie Y. Bishop, M.D., Juan E. Santiago-Torres, M.S., Nathan Rimmke, M.D., and David C. Flanigan, M.D.
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.
T
he prevalence of smoking remains close to 20% in the general population, being highest in persons below the poverty level or aged 22 to 44 years.1 Smoking has been strongly linked to cancer, chronic obstructive pulmonary disease, and cardiovascular disease.2 Smoking has also been shown to have adverse clinical musculoskeletal effects, including an increased risk of sustaining a fracture, nonunion and delayed union of fractures, and decreased bone mineral density.3 In addition, we recently showed in a systematic From the Department of Orthopaedics, The Ohio State University, Columbus, Ohio, U.S.A. The authors report the following potential conflict of interest or source of funding: D.C.F. receives support from Sanofi and Smith & Nephew. Received October 28, 2014; accepted January 21, 2015. Address correspondence to Julie Y. Bishop, M.D., Sports Medicine Center, The Ohio State University, 2050 Kenny Rd, Ste 3100, Columbus, OH 43221, U.S.A. E-mail: [email protected] Ó 2015 by the Arthroscopy Association of North America 0749-8063/14903/$36.00 http://dx.doi.org/10.1016/j.arthro.2015.01.026
review that smoking is associated with poor clinical outcomes after rotator cuff (RTC) repair and poor healing outcomes of small to medium tears.4 Because smoking temporarily decreases tissue oxygenation and nicotine is a potent vasoconstrictor, the effect of smoking may be marked in already hypovascular areas, such as the soft tissue within the shoulder.5 Hence it is reasonable to assume that smoking is associated with RTC pathology. Although individual studies have been published on the effects of smoking on normal shoulder tendon tissue, to date, there have been no comprehensive reviews of the literature on the topic. With the increasing life expectancy and as the baby boomer generation ages, orthopaedic surgeons are seeing more elderly patients presenting with degenerative RTC tears.6 Some studies suggest that the prevalence and extent of degenerative RTC tears increase with advancing age,7,8 highlighting the importance of addressing risk factors to prevent RTC tears. Therefore the purpose of this study was to investigate the
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association of smoking with RTC disease and shoulder dysfunction. We hypothesized that smoking has a negative effect on shoulder health.
Methods A systematic review was conducted according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines9 (Fig 1). The search strategy was based on “shoulder AND [smoke OR smoking OR nicotine OR tobacco].” The search was independently confirmed by the coauthors (J.Y.B., J.E.S-T., N.R., D.C.F.) on October 4, 2014. The following medical databases were used: PubMed, CINAHL (Cumulative Index to Nursing and Allied Health Literature), SPORTDiscus, and The Cochrane Library. We included studies with Levels I, II, III, and IV evidence as defined by the Oxford Centre for EvidenceBased Medicine and used by the American version of The Journal of Bone and Joint Surgery.10 Meeting and conference abstracts were not eligible for inclusion. The senior author (J.Y.B.) made the final decision on article inclusion if there was disagreement among authors. Top hits in Web search engines and all references within included studies were checked to identify potentially relevant studies missed by the initial database search. Any English-language clinical articles studying smoking and shoulder function assessed with shoulder rating scales or RTC or glenoid labrum disease with evidence Levels I through IV were included. Basic science studies analyzing the anatomy, histology, pathology, biomechanics, or imaging characteristics associated with RTC or glenoid labrum disorders were also included. The exclusion criteria consisted of noneEnglishlanguage studies and studies of Level V evidence (i.e., single-case report, expert opinion, or personal observation). Any clinical and basic science studies analyzing any joint other than the shoulder were also excluded. In addition, studies reporting only subjective pain findings or on adhesive capsulitis were excluded. Finally, studies reporting on fractures or oncologic masses around the shoulder were excluded, as were studies analyzing only the outcomes of surgery, without reporting preoperative status. Continuous variable data were reported as means and standard deviations from the means. Categorical variable data were reported as frequencies with percentages. Associations were reported as odds ratios (ORs) with corresponding 95% confidence intervals (CIs). P < .05 was considered significant.
Results Thirteen studies were identified for inclusion and analysis, comprising 16,172 patients, of whom 6,081 were smokers. Four of these studies were clinical
Fig 1. Search strategy according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines. Thirteen studies were identified for inclusion. No studies on smoking and glenoid labrum disease were found. (RTC, rotator cuff.)
studies that addressed the association between smoking and patient-reported shoulder dysfunction (i.e., poor scores on shoulder rating scales) and symptoms (Table 1). Another 4 clinical studies examined the correlation between smoking and provider-reported RTC disease (Table 2). The other studies investigated the relation of smoking and degree of RTC pathology or mechanical properties of the RTC (3 clinical, 1 cadaveric, and 1 basic science study) (Table 3). No studies specifically exploring the effects of smoking on the glenoid labrum were found. Patient-Reported Shoulder Symptoms and Dysfunction Smokers were more likely to report shoulder pain and decreased shoulder function (Table 1). With a total of 6,678 patients (mean age, 52 years), of whom 1,723 were smokers, all 4 clinical studies reviewed found a significant negative association between smoking and shoulder function and symptoms. McRae et al.11 performed a retrospective cohort study, which included 54 patients who underwent arthroscopic RTC repair, only 9 of whom were smokers. They found that smoking status was negatively correlated with preoperative Simple Shoulder Test scores (P ¼ .003). However, smoking status was not associated
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Table 1. Clinical Studies on Smoking and Patient-Reported Symptoms and Shoulder Dysfunction Journal J Shoulder Elbow Surg
No. of Patients (Mean Age, yr) 54 (58.2)
BMC Musculoskelet Disorders
6,237 (51.9)
Sports Health
163
Authors McRae et al.11 (2011)
Rechardt et al.12 (2010)
Kane et al.13 (2010)
Mallon et al.14 (2004)
J Shoulder Elbow Surg
224 (52.3)
Pertinent Findings Smoking was associated with poor shoulder function and pain scores. Smoking was correlated with SST scores (P ¼ .003) and had a greater correlation when combined with female sex and work-related injury (P < .001). However, there was no correlation with ASES scores (P ¼ .184). Patients with unilateral shoulder pain (OR, 1.9; 95% CI, 1.3 to 2.9) and bilateral shoulder pain (OR, 1.8; 95% CI, 1.0 to 3.1) were more likely to be currently smoking men who had smoked for >20 pack-years and women who had smoked for 10 to 20 packyears, respectively. Smoking was not associated with chronic RTC tendinitis. Shoulder pain and loss of function were found to be proportional to smoking. Smokers had worse mean scores on the Subjective Shoulder Rating System assessment (P ¼ .005), Shoulder Rating Questionnaire (P ¼ .0008), and Oxford Shoulder Questionnaire (P ¼ .0042). Smokers also reported lower active range of motion in both the left and right shoulders (P ¼ .024). No significant difference was found between smokers of <1 pack per day and smokers of 1 pack per day. Preoperative scores showed that smokers had higher pain scores (P < .0001) and lower UCLA scores (P ¼ .00025) than nonsmokers.
ASES, American Shoulder and Elbow Surgeons; CI, confidence interval; OR, odds ratio; RTC, rotator cuff; SST, Simple Shoulder Test; UCLA, University of California, Los Angeles shoulder scale.
with worse preoperative American Shoulder and Elbow Surgeons scores (P ¼ .184). Rechardt et al.12 interviewed and examined 6,237 patients, of whom 1,589 were smokers, to correlate
smoking and shoulder pain. This cross-sectional study found that current smoking status was associated with unilateral shoulder pain in men but not in women. The authors found that currently smoking men who had a
Table 2. Clinical Studies on Smoking and Provider-Reported Rotator Cuff Disease Authors Baumgarten et al.15 (2010)
Fehringer et al.16 (2008)
Tangtrakulwanich and Kapbird17 (2012)
Titchener et al.18 (2014)
Journal Clin Orthop Relat Res
J Shoulder Elbow Surg
World J Orthop
J Shoulder Elbow Surg
CI, confidence interval; OR, odds ratio; RTC, rotator cuff.
No. of Patients (Mean Age, yr) 584 (57.7)
104 (71.4)
302 (50)
7,471 (55)
Pertinent Findings This study showed a time- and dose-dependent relation between smoking and RTC tears. The correlation increased when smoking occurred within 10 yr of presentation (OR, 4.24; CI, 1.75 to 10.25; P ¼ .0006) and was significant in patients with a history of smoking 1 to 2 packs per day (OR, 1.66; P ¼ .009) and even greater for 2 packs per day (OR, 3.35; P ¼ .0007). Ultrasonography was used to diagnose RTC tears. No statistically significant association of smoking with increasing RTC tear prevalence was found (P ¼ .52) in 200 shoulders from 104 patients aged 65 yr. Ultrasonography was used to diagnose RTC tears. Current smokers were at greater risk of impingement syndrome compared with nonsmokers (OR, 6.8; 95% CI, 1.2 to 39). Impingement syndrome was diagnosed with a lidocaine subacromial injection test. Current smoking status was not associated with a diagnosis of RTC disease (OR, 1.03; CI, 0.91 to 1.15), whereas a history of smoking was associated with RTC disease (OR, 1.24; CI, 1.10 to 1.39). This effect disappeared after adjustment for number of general practice consultation rate per year (OR, 1.09; CI, 0.96 to 1.23).
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Table 3. Studies on Smoking and Degree of Rotator Cuff Pathology
Journal
Type of Study or No. of Patients (Mean Age, yr)
Pertinent Findings
Animal model (rat)
Nicotine caused an increase in the calculated elastic modulus of the supraspinatus tendon (P < .05).
Authors Basic science study Ichinose et al.19 (2010)
Acta Orthop
Clinical studies Carbone et al.20 (2012)
J Shoulder Elbow Surg
Kane et al.21 (2006)
Orthopedics
Cadaveric study, 36 (75)
Kukkonen et al.22 (2014)
Scand J Med Sci Sports
564 (59.8)
Lundgreen et al.23 (2014)
Arthroscopy
25 (55.6)
408 (59)
The analysis resulted in a finding suggestive of significance of an increase in the severity of RTC tears as the average number of cigarettes smoked increased (P ¼ .099). When combining type II, III, and IV tears (SCOI classification), the authors showed that increasing tear severity was associated with increasing daily numbers of cigarettes (P ¼ .04). In addition, the total number of cigarettes smoked over a lifetime differed significantly between patients with a small tear and those with at least a type II tear (P ¼ .032). Macroscopic RTC tears were more likely in cadavers with a history of smoking, and the presence of advanced microscopic RTC pathology was more than twice as likely in cadavers with a history of smoking. The data were not statistically significant. Smokers were significantly younger, with equally large tears, compared with nonsmokers (P < .001). There was no significant difference in preoperative Constant score (P ¼ .075) or mean size of intraoperatively measured tendon tear (P ¼ .5) in smokers v nonsmokers. Samples of the supraspinatus muscle were obtained arthroscopically in patients undergoing surgery for full-thickness RTC tears. Those with a smoking history of at least half a pack per day had a longer duration of symptoms (19 months v 11 months, P < .05), were younger (52 yr [SD, 6.4 yr] v 58 yr [SE, 5.8 yr]; P < .01), and had more advanced degeneration with a higher Bonar score (13.5 v 9, P < .001) than nonsmokers. The study also showed increased density of apoptotic cells (P < .024), reduced tenocyte density (P < .019), and upregulation of proliferative activity (P < .0001) in tendons of patients with a smoking history.
RTC, rotator cuff; SCOI, Southern California Orthopedic Institute.
history of smoking of more than 20 pack-years were at the highest risk of unilateral shoulder pain (OR, 1.9; 95% CI, 1.3 to 2.9). Currently smoking women who had a history of smoking of 10 to 20 pack-years were at highest risk of bilateral shoulder pain (OR, 1.8; 95% CI, 1.0 to 3.1). Smoking was not found to be associated with the presence of chronic RTC tendinitis. Self-reported shoulder surveys have also found a correlation between smoking and shoulder dysfunction. Kane et al.13 provided a subjective assessment of shoulder function using 3 different patient-response surveys, answered by 163 patients. The Oxford Shoulder Questionnaire (P ¼ .0042), the Shoulder Rating Questionnaire (P ¼ .0008), and the Subjective Shoulder Rating System (P ¼ .005) all found smokers (n ¼ 30) to have worse shoulder function than nonsmokers (n ¼ 133). In addition, smokers reported higher complaints of pain (P ¼ .04) and lower active range of motion (P ¼ .024). In addition, smoking status has been shown to have a negative effect on patients with RTC tendon tears. Mallon et al.14 studied 224 patients and reported that
smokers (n ¼ 95) had higher preoperative pain scores (P < .0001) and lower preoperative University of California, Los Angeles scores (P ¼ .00025) than nonsmokers (n ¼ 129). Provider-Reported RTC Disease Mixed results were found in the 4 clinical studies reviewed on smoking and provider-reported RTC disease, comprising 8,461 patients, of whom 4,082 were smokers (Table 2). Two of these studies used ultrasonography to assess the prevalence of RTC tears. Baumgarten et al.15 found a dose-dependent and time-dependent relation between smoking and RTC tears. They analyzed 584 patients, of whom 473 were smokers, who underwent a diagnostic shoulder ultrasound for unilateral, atraumatic shoulder pain with no history of shoulder surgery. They reported RTC tears to be more prevalent in patients with a history of smoking (P ¼ .002) and in those with a history of smoking within 10 years of presentation (P ¼ .0006). They also found that the RTC tear cohort had a higher rate of tobacco use in terms of the mean number of packs per day (P ¼ .004), a
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longer duration of smoking (P ¼ .05), and a larger tobacco exposure (P ¼ .0006). Fehringer et al.16 also used ultrasonography to determine the prevalence of RTC tears and found contrasting results to those of Baumgarten et al. No statistically significant association of smoking with increasing RTC tear prevalence was found in 200 shoulders of 104 patients aged 65 years or older, of whom 78 had a smoking history (P ¼ .52). Tangtrakulwanich and Kapbird17 performed a casecontrol study that evaluated the association between smoking and impingement syndrome in 302 patients. Patients who currently smoked (n ¼ 26) had a 6.8 times greater risk of impingement syndrome than nonsmokers (OR, 6.8; 95% CI, 1.2 to 39). Impingement syndrome was diagnosed with a lidocaine subacromial injection test. In a large case-control study, Titchener et al.18 looked at 5,000 patients with RTC disease and 5,000 controls. Smoking data were available for 78.9% of cases and 70.5% of controls, for a total of 7,471 patients, of whom 3,505 had a smoking history. Current smoking status (n ¼ 1,761) was not associated with a diagnosis of RTC disease (OR, 1.03; 95% CI, 0.91 to 1.15). A history of smoking (n ¼ 1,744) was associated with RTC disease (OR, 1.24; 95% CI, 1.1 to 1.39), although this effect disappeared after adjustment for yearly rate of number of patient visits to a general practitioner (OR, 1.09; 95% CI, 0.96 to 1.23). Mechanical Properties and Degree of RTC Pathology The literature has also shown a link between smoking and the degree of RTC pathology. Four of five studies reviewed on this topic found a statistically significant correlation between the two (Table 3). Ichinose et al.19 performed a basic science study in which they randomized 27 rats to 3 groups. Over a 12week period, a subcutaneously implanted osmotic pump delivered either a high-dose nicotine solution (45 ng/mL), a low-dose nicotine solution (22.5 ng/mL), or saline solution (controls). The authors found that the elastic modulus of the supraspinatus tendon in the high- and low-dose groups was higher than that in the control group (P ¼ .04 and P ¼ .03, respectively). A higher elastic modulus in a tendon indicates that it is stiffer and more susceptible to injury. Carbone et al.20 found a correlation among cigarette smoking, presence of RTC tears, and RTC tear size. Their study comprised 408 patients, of whom 131 were smokers, who underwent arthroscopic RTC repair. The RTC tears were classified intraoperatively according to the Southern California Orthopedic Institute classification system24: type I tears are small, complete tears, such as a puncture wound; type II tears are moderate tears (<2 cm) that encompass only 1 tendon, with no retraction of the tendon ends; type III tears are large (3
5
to 4 cm), with minimal retraction of the torn edge; and type IV tears are massive tears, involving 2 or more tendons and associated with retraction and scarring, and are frequently irreparable. Carbone et al. showed that the frequency of smokers was 23.2% among patients with a small full-thickness tear in contrast to 34.8% among those with a larger full-thickness tear (P ¼ .033). When combining type II, III, and IV tears, they found an increasing severity of tears associated with an increasing daily number of cigarettes (P ¼ .04). In addition, the total number of lifetime cigarettes smoked was significantly higher in patients with at least a type II tear (P ¼ .032). Kukkonen et al.22 looked at preoperative data for 564 consecutive shoulders undergoing arthroscopic repair for RTC tears. They found a statistically significant difference in the mean age of smokers (55 years; SD, 9.1 years; n ¼ 114) compared with nonsmokers (61 years; SD, 9.4 years; n ¼ 450) at the time of surgery (P < .001). There was no difference in the size of the tear between groups. Although the pack-years of smoking did not statistically correlate with preoperative Constant scores (P ¼ .075), the data suggest that smoking is a risk factor for tears at a younger age. Kane et al.21 did not find a statistically significant correlation between the incidence of RTC disease and smoking, although there was a strong trend toward such a finding. They dissected 72 shoulders in 36 cadavers to identify microscopic and macroscopic evidence of RTC disease. They also looked at microscopic samples of lung tissue from each cadaver to determine smoking history, identifying 21 of the cadavers as smokers. Of the 72 shoulders, 36 had evidence of macroscopic RTC disease (full- or partial-thickness RTC tear on gross visualization), and 23 of these had evidence of a smoking history compared with only 13 that had no evidence of a smoking history. Microscopic evidence of RTC disease (grade 3 or 4 fibrous degeneration) was more than twice as likely in cadavers with evidence of a smoking history. Again, although there were strong trends, none of these data were statistically significant. Lundgreen et al.23 found a statistically significant association of smoking with symptoms, tear at a younger age, and worsened histopathology of the supraspinatus tendon in 25 patients, of whom 10 were smokers. Samples of the supraspinatus muscle were obtained arthroscopically in patients undergoing arthroscopic surgery for full-thickness RTC tears. Those with a smoking history of at least half a pack per day were found to have a longer duration of symptoms (19 months v 11 months, P < .05) and had more advanced degeneration with a higher Bonar score (13.5 v 9, P < .001) than nonsmokers. In addition, the patients with a smoking history were younger than the nonsmokers (52 years [SD, 6.4 years] v 58 years [SE,
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5.8 years]; P < .01). Lundgreen et al. also showed increased density of apoptotic cells (P < .024), reduced tenocyte density (P < .019), and upregulation of proliferative activity (P < .0001) in tendons of patients with a smoking history.
Discussion Our systematic review confirmed that smoking has a negative influence on the health of the shoulder. Specifically, we report that smoking is associated with a higher prevalence of symptomatic shoulder disease and dysfunction (i.e., poor scores on shoulder rating scales), risk of RTC degeneration, and larger RTC tears, as well as an increased risk of tears at a younger age. The current literature shows mixed results regarding whether smokers have a higher overall prevalence of RTC tendon tears. This study found that smokers have higher amounts of shoulder pain and worse shoulder function than nonsmokers as assessed with the Shoulder Simple Test; University of California, Los Angeles shoulder scale; and self-reported shoulder surveys. Smoking increases the number of circulating proinflammatory cytokines, and this may prolong inflammation and increase sensitivity to pain.25-27 Shoulder diseases, such as RTC lesions and subacromial bursitis, have been associated with increased expression of these cytokines.28-33 These findings suggest that smoking could lead to an increased need for treatment because it increases the risk of symptomatic shoulder disease. Determining what kind of treatment is necessary is difficult because we do not have any controlled data regarding how well smokers respond to nonoperative management of RTC disease. In addition, Mallon et al.14 showed that smoking status has negative effects on patients with proven RTC tears. Thus this finding further reinforces the idea that smokers are less likely to cope and undergo successful nonoperative treatment. This is a major clinical concern for shoulder surgeons because it has been proved in the literature that smoking leads to poor clinical and healing outcomes of RTC repair.4 In addition, some studies have shown that the patients who benefit most from arthroscopic RTC repair have good preoperative strength.34 If we use preoperative functional status as a predictor of surgical outcome, smokers will have worse surgical outcomes. The literature is less clear on how smoking affects the prevalence of RTC disease. Baumgarten et al.,15 Carbone et al.,20 and Tangtrakulwanich and Kapbird17 did show an association between smoking and the prevalence of RTC tears and impingement syndrome, whereas Fehringer et al.,16 Titchener et al.,18 and Kane et al.21 did not. Baumgarten et al. and Fehringer et al. both used ultrasonography to detect the prevalence of RTC tears. Ultrasound has been shown to be 96% accurate, 100% sensitive, and 85% specific for diagnosing
full-thickness RTC tears.35 However, the sensitivity drops to 67%, with the specificity remaining at 85%, when diagnosing partial-thickness RTC tears. This may decrease the validity of the results of Baumgarten et al. and Fehringer et al. Titchener et al. used a database to identify patients with a diagnosis code related to RTC disease. They did not specify how they determined the diagnosis, and thus we cannot comment on the accuracy of their results. The gold standard to identify the presence of an RTC tear is either diagnostic arthroscopy or open dissection, and only 2 studies included in our literature review used these diagnostic modalities. Carbone et al. used arthroscopy to show that smokers do have a higher prevalence of RTC tears. In addition, Kane et al. showed a strong trend linking smoking and RTC disease through cadaveric dissections, although their data did not reach statistical significance likely because not enough cadavers were included in the study and, hence, the power was insufficient. Carbone et al.,20 Kukkonen et al.,22 Kane et al.,21 and Lundgreen et al.23 showed a link between smoking and increasing degree of RTC pathology. Their studies confirmed that smokers have larger tears, higher grades of fibrous degeneration, and increased numbers of tears at a younger age. These findings are of clinical importance because larger RTC tears have a more unfavorable treatment history. This is because RTC tears are associated with higher retear rates than smaller tears after repair.36-38 Furthermore, smoking has been shown to decrease cuff healing4; thus smokers with larger tears are at an additional disadvantage regarding healing of the repair. Although many unhealed RTC repairs have been found to be clinically asymptomatic,39,40 one could surmise from the data presented in our review that smokers tend to have more RTC-related pain and perhaps would have more symptomatic unhealed RTC repairs. In addition, postoperative strength and function are worse after repair of large and massive RTC tears as compared with small tears.41 These findings should prompt the surgeon to take smoking status into consideration when assessing the prognosis for a patient undergoing an RTC repair procedure. The results discussed in this report are biologically plausible because vascular insufficiency to the critical portions of the shoulder are implicated in the genesis of RTC tears.42 Anatomic and histologic studies have confirmed a region of relative hypovascularity within the tendons of the supraspinatus and infraspinatus just proximal to their insertion on the greater tuberosity.42-44 Tobacco smoking likely contributes to the tendon degeneration processes because nicotine causes hypoxia, limiting blood supply to the hypovascular portion of the RTC.42 This hypoxic environment may lead to altered metabolism and a decreased healing response. In fact, Lundgreen et al.23 found increased density of apoptotic cells and reduced density of tenocytes in torn RTCs of
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patients with a smoking history. Another factor that could lead to pathologic processes in the shoulder is that smoking can change the mechanical properties of the RTC tendon. Ichinose et al.19 showed that tendons exposed to nicotine had a higher elastic modulus than controls. It has been previously shown that RTC tears commonly start at the anterior third of the supraspinatus tendon, where the elastic modulus is the highest.45-47 The aforementioned finding suggests that smoking increases the likelihood of an RTC tear by increasing the elastic modulus of the tendon. Ichinose et al. speculated that nicotine may increase the stiffness of the tendon through increased synthesis of collagen and reduced production of matrix metalloproteinase. No basic science studies were found that explored the effects of other toxins in cigarette smoke on the soft tissue of the shoulder. Therefore further study would potentially elucidate the causative components of tobacco smoke and the biochemical and pathophysiologic mechanisms in the setting of RTC pathology, which are essential in understanding whether nicotine replacement therapy is a viable option for patients at risk of RTC pathology. Limitations This systematic review has some limitations to consider. The literature meeting the inclusion criteria were only retrospective studies. Recall bias from patients perceiving smoking as the cause of their illness could have a significant impact on our results; hence prospectively designed studies could be of benefit. Studies performed in the hospital setting could result in selection bias toward patients with poor health, and those recruiting only from referral centers do not provide a true cross section of the population. Moreover, the use of only 1 ultrasonographer in some studies and differences between interviewers could result in observation bias. Some potential confounders are occupation and activity level, whereas age was controlled for in all the studies. In addition, a source of selection bias is inherent because only English-language studies were included. This review examined only tobacco smoking, not smokeless tobacco or nicotine patches or gum. In this study we did not control for the clinical measurements used, different criteria for inclusion as a smoker, and method for assessing RTC disease. Only 2 studies assessed tears intraoperatively, and 2 other studies used ultrasound, which has a high sensitivity and specificity for fullthickness tears but a lower sensitivity for partialthickness tears.35 None of the studies included were performed in developing countries. As a consequence of these limitations, it is challenging to draw generalizable conclusions from the studies.
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.
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