Abstract
Background:
Certain metabolic factors have been proposed as risk factors for a posterosuperior rotator cuff tear. Although metabolic syndrome is of increasing concern in industrialized societies, little information exists regarding its association with posterosuperior rotator cuff tears. The purpose of this study was to determine the risk factors for an atraumatic posterosuperior rotator cuff tear, including metabolic factors and metabolic syndrome.
Methods:
This study involved 634 subjects (634 shoulders) drawn from a cohort of rural residents. Posterosuperior rotator cuff tear diagnoses were based on magnetic resonance imaging (MRI) findings. Logistic regression analysis was used to determine the odds ratios (ORs) and 95% confidence intervals (CIs) for various demographic, physical, and social factors, including age, sex, dominant-side involvement, body mass index (BMI), and participation in manual labor; the comorbidities of diabetes, hypertension, dyslipidemia, thyroid dysfunction, ipsilateral carpal tunnel syndrome, and metabolic syndrome; and the serum metabolic parameters of serum lipid profile, glycosylated hemoglobin A1c, and level of thyroid hormone. Two multivariable analyses were performed: the first excluded metabolic syndrome while including diabetes, hypertension, BMI, and hypo-high-density lipoproteinemia (hypo-HDLemia), and the second included metabolic syndrome while excluding the formerly included variables.
Results:
Age, BMI, waist circumference, dominant-side involvement, manual labor, diabetes, hypertension, metabolic syndrome, ipsilateral carpel tunnel syndrome, HDL (high-density lipoprotein), and hypo-HDLemia were significantly associated with posterosuperior rotator cuff tears in univariate analyses (p ≤ 0.035). In the first multivariable analysis, age (OR. 1.86 [95% CI, 1.47 to 2.35]), BMI (OR, 1.09 [95% CI, 1.02 to 1.18]), dominant-side involvement (OR, 2.04 [95% CI, 1.38 to 3.01]), manual labor (OR, 9.48 [95% CI, 5.13 to 17.51]), diabetes (OR, 3.38 [95% CI, 1.98 to 5.77]), and hypo-HDLemia (OR, 2.07 [95% CI, 1.30 to 3.29]) were significantly associated with posterosuperior rotator cuff tears (p ≤ 0.019). In the second multivariable analysis, age (OR, 1.85 [95% CI, 1.48 to 2.31]), dominant-side involvement (OR, 1.83 [95% CI, 1.26 to 2.67]), manual labor (OR, 7.71 [95% CI, 4.33 to 13.73]), and metabolic syndrome (OR, 1.98 [95% CI, 1.35 to 2.91]) were significantly associated with posterosuperior rotator cuff tears (p ≤ 0.002).
Conclusions:
The metabolic factors of diabetes, BMI, hypo-HDLemia, and metabolic syndrome were significant independent factors associated with the development of posterosuperior rotator cuff tears.
Level of Evidence:
Prognostic Level III. See Instructions for Authors for a complete description of levels of evidence.
Rotator cuff tears are the most common disease entity in the shoulder and a notable source of shoulder disability. The posterosuperior rotator cuff, composed of the supraspinatus and the infraspinatus tendons, is the most common site of a rotator cuff tear. Extrinsic and intrinsic causes have been proposed to explain rotator cuff tears. However, the causes of posterosuperior rotator cuff tears are multifactorial and have not yet been clearly elucidated1,2. Most of the subjects in previous relevant studies, including most of the control groups, have been patients of clinics or hospitals rather than subjects recruited from the general population. Some recent studies have proposed age2, activity3, and genetics4 as well as the following metabolic factors, among others, as risk factors for rotator cuff tear: obesity5,6, dyslipidemia7,8, hyperglycemia9, thyroid functional abnormalities10, and diabetes11. Many of these metabolic factors remain unconfirmed or controversial as posterosuperior rotator cuff tear risk factors7,8,12. Additionally, little information exists regarding any association of those metabolic factors with posterosuperior rotator cuff tears in the general population.
Metabolic syndrome is a clustering of medical conditions including dyslipidemia (hypertriglyceridemia [hyper-TGmia] or hypo-high-density lipoproteinemia [hypo-HDLemia]), hypertension, hyperglycemia, and abdominal obesity. This syndrome is related to various chronic degenerative diseases, including cardiovascular disease, stroke, diabetes, and osteoarthritis13. Metabolic syndrome is of growing concern in industrialized societies because of its high prevalence and the serious morbidity associated with the syndrome; however, there have been few studies that have investigated associations between metabolic syndrome and musculoskeletal disorders. One study reported metabolic syndrome as a risk factor for shoulder pain without confirming rotator cuff integrity with diagnostic imaging or arthroscopy14. Therefore, it is not clear whether metabolic syndrome is a risk factor for rotator cuff tears.
The purpose of the current study was to investigate the strengths of the associations between atraumatic posterosuperior rotator cuff tears and various factors, including metabolic factors and metabolic syndrome, in a general population.
Materials and Methods
This study received institutional review board approval. A total of 1,149 volunteers, all of whom lived in the studied rural region, were recruited and enrolled; they constituted this study’s cohort. The volunteer participants completed a questionnaire and underwent physical examination of both shoulders by an orthopaedic surgeon (J.-Y.G.), fasting blood testing, radiographic evaluation of both shoulders (true anteroposterior, axillary lateral, and outlet views), bilateral shoulder magnetic resonance imaging (MRI), and bilateral upper-extremity electrophysiological assessment.
Inclusion criteria required subjects to sign an informed consent document and to have a complete clinical evaluation as described above. MRI evaluations were performed using a 1.5-T scanner (Siemens Medical Systems). Four sequences (each with a slice thickness of 3 mm, a field of view from 15.9 to 18.0 cm, and 1 excitation) were obtained, as follows: (1) oblique sagittal T1-weighted spin-echo (TR/TE [repetition time/echo time] = 452/11 ms, matrix size of 192 × 320); (2) oblique sagittal T2-weighted turbo-spin-echo (TSE) with fat saturation (TR/TE = 2,800/56 ms, matrix size of 269 × 448); (3) oblique coronal T2-weighted TSE with fat saturation (TR/TE = 2,800/56 ms, matrix size of 269 × 448); and (4) axial T2-weighted TSE with fat saturation (TR/TE = 2,800/56 ms, matrix size of 267 × 384).
Five hundred and fifteen subjects were excluded for the following reasons: the absence of a complete MRI study (17 subjects, 33 shoulders); history of shoulder trauma or surgery, osteoarthritis, calcific tendinitis, frozen shoulder, or subscapularis tendon tear (380 subjects, 760 shoulders); and current medication that might have affected serum lipid levels (118 subjects, 236 shoulders) (Fig. 1). Only 1 shoulder per subject was included in our analysis. In cases with either bilateral posterosuperior rotator cuff tears or no posterosuperior rotator cuff tear, 1 shoulder was randomly excluded (using random number generation). For subjects with a unilateral posterosuperior rotator cuff tear, only the involved shoulder was included. Therefore, the total number of subjects included in our analysis was 634 (634 shoulders).
Fig. 1.
Flowchart showing exclusion and inclusion criteria for this study. All 634 subjects met our inclusion criteria.
We diagnosed a posterosuperior rotator cuff tear as either a partial-thickness or full-thickness tear, on the basis of MRI findings. High signal intensity within the cuff tendon that extended to the bursal or articular surface indicated a partial-thickness tendon tear. High signal intensity passing through the entire thickness of the tendon indicated a full-thickness tear15. The radiologist (J.B.N.) who diagnosed the tear was blinded to patients’ laboratory and other clinical data.
The demographic factors that were evaluated were sex and age. The physical factors that were evaluated included height, weight, body mass index (BMI), waist circumference, and dominant-side involvement. The social factors that were considered were smoking, alcohol consumption, and participation in labor according to the volunteer’s occupation. To facilitate interpretation and to clarify the association between increasing age and higher rotator cuff tear prevalence, we divided age into 5 categories: <40, 40 to 49, 50 to 59, 60 to 69, and ≥70 years of age. The investigated medical comorbidities were diabetes, hypertension, metabolic syndrome, hyper- and hypothyroidism, and ipsilateral carpal tunnel syndrome. We accepted prior diagnoses of diabetes, and we diagnosed new cases of diabetes on the basis of the finding of a serum glycosylated hemoglobin A1c (HbA1c) level of >6.4%. Hypertension was diagnosed according to previous medical history or the detection of a blood pressure level of >140 mm Hg for systolic or >90 mm Hg for diastolic pressure16. Clinical identification of metabolic syndrome was based on a subject’s meeting 3 of the following 5 criteria: (1) a fasting plasma glucose level of ≥100 mg/dL or taking antidiabetic medication; (2) systolic blood pressure of ≥130 mm Hg, diastolic blood pressure of ≥85 mm Hg, or taking antihypertensive medication; (3) a serum triglyceride (TG) level of ≥150 mg/dL; (4) a serum high-density lipoprotein (HDL) level of <40 mg/dL for men or <50 mg/dL for women; and (5) a waist circumference of ≥90 cm for men or ≥85 cm for women17,18. The waist circumference criteria for obesity were adjusted according to Korean norms19. We also accepted prior diagnoses of hyper- and hypothyroidism as well as diagnosed additional cases of hyper- and hypothyroidism according to the results of thyroid function tests for which a serum free thyroxine (T4) level of >1.70 ng/dL indicated hyperthyroidism and a level of <0.93 ng/dL indicated hypothyroidism20.
Prior studies have noted that carpal tunnel syndrome is associated with rotator cuff tears11,21. Therefore, we included the results of our carpal tunnel syndrome evaluations of all enrolled subjects. Carpal tunnel syndrome was diagnosed according to electrophysiological findings, after consideration of symptoms and findings on physical examination. Electrophysiological diagnosis was based on established criteria: a median nerve distal motor latency of >4.0 ms, distal sensory latency of >3.6 ms, or a distal sensory latency delay of >0.5 ms as compared with conduction measurements of the median nerve and the ulnar nerve in the fourth digit22.
Serum lipid profiles were evaluated as scale and categorical variables. The scale variables were total cholesterol, low-density lipoprotein (LDL), TG, HDL, and non-HDL levels. The categorical variables included the following dyslipidemias: hypercholesterolemia (total cholesterol of ≥200 mg/dL), hyper-LDLemia (LDL of ≥100 mg/dL), hyper-TGmia (TG of ≥150 mg/dL), hypo-HDLemia (HDL of <40 mg/dL for men and <50 mg/dL for women), and hyper-non-HDLemia (non-HDL of ≥130 mg/dL). High-sensitivity C-reactive protein (hs-CRP) was also evaluated.
Statistical Analysis
The associations between posterosuperior rotator cuff tears and specific factors, including general physical factors, social factors, comorbidities, and serum lipid profiles, were evaluated by calculating the odds ratios (ORs) with 95% confidence intervals (CIs) using logistic regression analyses. Univariate logistic regression analyses were performed for all variables; multiple logistic regression analyses were then performed on variables demonstrating significant associations. Because metabolic syndrome possibly has multicollinearity with BMI, diabetes, hypertension, and hypo-HDLemia, we performed 2 different multivariable analyses after assessment of multicollinearity, using factors with a variance inflation factor (VIF) and a conditional index. Multicollinearity was considered absent when both the VIF and conditional index were <1023. Goodness of fit for the multivariable logistic regression model was determined by the Hosmer-Lemeshow test. All statistical analyses were performed using SPSS software (version 21.0; IBM). Significance for the logistic analyses was set at the level of p < 0.05. Significance for the Hosmer-Lemeshow test was set at p > 0.05.
Results
The 634 subjects had a mean age (and standard deviation) of 59.1 ± 8.6 years. Among the 327 female participants (51.6%), the mean age was 58.3 ± 8.3 years, and among the 307 male participants (48.4%), it was 59.9 ± 8.9 years. Age-related data are summarized in Table I.
TABLE I.
Data on Age and Sex According to Occupation of Enrolled Subjects*
| No. (%) | Mean Age ± SD (yr) | |
| Total enrolled | 634 (100%) | 59.1 ± 8.6 |
| Male | 307 (48.4%) | 59.9 ± 8.9 |
| Female | 327 (51.6%) | 58.3 ± 8.3 |
| Agricultural worker | 456 (71.9%) | 58.8 ± 8.9 |
| Male | 216 (47.4%) | 59.4 ± 9.1 |
| Female | 240 (52.6%) | 58.2 ± 8.7 |
| Office worker | 178 (28.1%) | 59.8 ± 7.9 |
| Male | 91 (51.1%) | 61.1 ± 8.5 |
| Female | 87 (48.9%) | 58.4 ± 6.9 |
For the values for male and female, the percentage is of the given group (total enrolled, agricultural worker, or office worker). SD = standard deviation.
The prevalence of posterosuperior rotator cuff tears was 31.4% (199 of 634). Of the 634 subjects, 11.2% (71) had a full-thickness posterosuperior rotator cuff tear and 20.2% (128) had a partial-thickness tear. The prevalence of symptomatic posterosuperior rotator cuff tears, according to the criteria of Moosmayer et al.24, was 22.6% (143 of 634). The prevalence data for all participants with a complete MRI study and for the subjects who were ultimately included in our analysis are summarized in Table II.
TABLE II.
Prevalence of Posterosuperior Rotator Cuff Tear (PSRCT)*
| Subjects with Complete MRI Study | Subjects Meeting All Inclusion Criteria | |
| PSRCT | 46.7% (529) | 31.4% (199) |
| Full-thickness | 17.4% (197) | 11.2% (71) |
| Partial-thickness | 29.3% (332) | 20.2% (128) |
| Symptomatic PSRCT† | 27.9% (316) | 22.6% (143) |
| Full-thickness | 12.0% (136) | 10.7% (68) |
| Partial-thickness | 15.9% (180) | 11.8% (75) |
| Bilateral PSRCT | 22.1% (250) | 14.5% (92)‡ |
A total of 1,132 subjects had complete MRI studies, and 634 met all inclusion criteria. The values are given as the percentage, with the number of subjects in parentheses.
Subjects with symptomatic PSRCT were identified using the criteria of Moosmayer et al.24.
The bilateral percentage came from data compiled before we excluded 1 shoulder for each of the 634 subjects.
Demographic data and the prevalence, mean, or median for each of the studied variables are summarized in Table III.
TABLE III.
Summary of Demographic Data and Values (Prevalence, Mean, or Median) for Studied Variables*
| Studied Variable | All Included | PSRCT Group | Intact Group |
| Male sex | 307 (48.4%) | 107 (53.8%) | 200 (46.0%) |
| Age† (yr) | 59.1 ± 8.6 | 61.9 ± 7.6 | 57.7 ± 8.8 |
| No. (%) by age by category | |||
| <40 yr | 8 (1.3%) | 0 (0.0%) | 8 (1.8%) |
| 40 to 49 yr | 66 (10.4%) | 11 (5.5%) | 55 (12.6%) |
| 50 to 59 yr | 265 (41.8%) | 66 (33.2%) | 199 (45.7%) |
| 60 to 69 yr | 218 (34.4%) | 86 (43.2%) | 132 (30.3%) |
| ≥70 yr | 77 (12.1%) | 36 (18.1%) | 41 (9.4%) |
| Height‡ (cm) | 161 (155-168) | 162 (155-167) | 161 (155-168) |
| Weight† (kg) | 63 ± 9 | 64 ± 10 | 62 ± 9 |
| BMI† (kg/m2) | 24 ± 3 | 25 ± 3 | 24 ± 3 |
| Waist circumference† (cm) | 84 ± 8 | 86 ± 8 | 84 ± 8 |
| No (%) by higher categories of waist circumference | |||
| 85-89.9 cm (women), 90-94.9 cm (men) | 128 (20.2%) | 35 (17.6%) | 93 (21.4%) |
| 90-94.9 cm (women), 95-99.9 cm (men) | 93 (14.7%) | 36 (18.1%) | 57 (13.1%) |
| ≥95 cm (women), ≥100 cm (men) | 33 (5.2%) | 14 (7.0%) | 19 (4.4%) |
| Dominant-side involvement | 314 (49.5%) | 122 (61.3%) | 192 (44.1%) |
| Smoking | 211 (33.3%) | 76 (38.2%) | 135 (31.0%) |
| Alcohol consumption | 424 (66.9%) | 123 (61.8%) | 301 (69.2%) |
| Manual labor | 456 (71.9%) | 183 (92.0%) | 273 (62.8%) |
| Diabetes | 92 (14.5%) | 51 (25.6%) | 41 (9.4%) |
| Hypertension | 174 (27.4%) | 66 (33.2%) | 108 (24.8%) |
| Metabolic syndrome | 210 (33.1%) | 89 (44.8%) | 121 (27.8%) |
| Hyperthyroidism | 10 (1.6%) | 3 (1.5%) | 7 (1.6%) |
| Hypothyroidism | 17 (2.7%) | 5 (2.5%) | 12 (2.8%) |
| Ipsilateral carpal tunnel syndrome | 142 (22.4%) | 55 (27.6%) | 87 (20.0%) |
| Serum lipid levels (mg/dL) | |||
| Total cholesterol† | 198 ± 37 | 200 ± 35 | 198 ± 37 |
| LDL† | 132 ± 34 | 133 ± 33 | 131 ± 34 |
| TG‡ | 107 (79-152) | 109 (83-160) | 104 (78-150) |
| HDL‡ | 55 (46-66) | 54 (45-63) | 57 (46-67) |
| Non-HDL† | 141 ± 36 | 145 ± 35 | 140 ± 37 |
| Dyslipidemia | |||
| Hypercholesterolemia | 292 (46.1%) | 95 (47.7%) | 197 (45.3%) |
| Hyper-LDLemia | 525 (82.8%) | 170 (85.4%) | 355 (81.6%) |
| Hyper-TGmia | 176 (27.8%) | 65 (32.7%) | 111 (25.5%) |
| Hypo-HDLemia | 137 (21.6%) | 62 (31.2%) | 75 (17.2%) |
| Hyper-non-HDLemia | 396 (62.5%) | 131 (65.8%) | 265 (60.9%) |
| hs-CRP‡ (mg/L) | 1 (0-1) | 1 (0-1) | 1 (0-1) |
A total of 634 subjects were included, including 199 in the posterosuperior rotator cuff tear (PSRCT) group and 435 in the intact group. The values are given as the number, with the percentage in parentheses, or as otherwise noted.
The values are given as the mean and standard deviation.
The values are given as the median, with the interquartile range in parentheses.
In univariate analyses, age, BMI, waist circumference, dominant-side involvement, manual labor, diabetes, hypertension, metabolic syndrome, ipsilateral carpal tunnel syndrome, HDL, and hypo-HDLemia were significant variables. The ORs for all variables, with 95% CIs, are presented in Table IV.
TABLE IV.
Strengths of Associations Between Studied Variables and Posterosuperior Rotator Cuff Tear in Univariate Analyses
| Studied Variable | OR (95% CI) | P Value |
| Male sex | 1.37 (0.98-1.91) | 0.069 |
| Age | 1.75 (1.43-2.14) | <0.001* |
| BMI (kg/m2) | 1.10 (1.04-1.18) | 0.002* |
| Waist circumference | 1.03 (1.01-1.06) | 0.003* |
| Dominant-side involvement | 2.01 (1.42-2.82) | <0.001* |
| Smoking | 1.37 (0.97-1.95) | 0.076 |
| Alcohol consumption | 0.72 (0.51-1.02) | 0.067 |
| Manual labor | 6.79 (3.93-11.73) | <0.001* |
| Diabetes | 3.31 (2.11-5.21) | <0.001* |
| Hypertension | 1.50 (1.04-2.17) | 0.030* |
| Metabolic syndrome | 2.10 (1.48-2.98) | <0.001* |
| Hyperthyroidism | 0.94 (0.24-3.66) | 0.924 |
| Hypothyroidism | 0.91 (0.32-2.61) | 0.859 |
| Ipsilateral carpal tunnel syndrome | 1.53 (1.04-2.26) | 0.033* |
| Total cholesterol (mg/dL) | 1.00 (1.00-1.01) | 0.531 |
| LDL (mg/dL) | 1.00 (1.00-1.01) | 0.469 |
| TG (mg/dL) | 1.00 (1.00-1.00) | 0.339 |
| HDL (mg/dL) | 0.99 (0.98-1.00) | 0.035* |
| Non-HDL (mg/dL) | 1.00 (1.00-1.01) | 0.133 |
| Hypercholesterolemia | 1.10 (0.79-1.55) | 0.566 |
| Hyper-LDLemia | 1.32 (0.83-2.10) | 0.238 |
| Hyper-TGmia | 1.42 (0.98-2.04) | 0.063 |
| Hypo-HDLemia | 2.17 (1.47-3.21) | <0.001* |
| Hyper-non-HDLemia | 1.24 (0.87-1.76) | 0.236 |
| hs-CRP (mg/L) | 1.04 (0.98-1.11) | 0.185 |
Significant.
For the first multivariable analysis, we excluded metabolic syndrome and included BMI, diabetes, hypertension, and hypo-HDLemia as well as age, dominant-side involvement, manual labor, and ipsilateral carpal tunnel syndrome; no multicollinearity among the 8 studied variables was shown. Age (OR, 1.86 [95% CI, 1.47 to 2.35]; p < 0.001), BMI (OR, 1.09 [95% CI, 1.02 to 1.18]; p = 0.019), dominant-side involvement (OR, 2.04 [95% CI, 1.38 to 3.01]; p < 0.001), manual labor (OR, 9.48 [95% CI, 5.13 to 17.51]; p < 0.001), diabetes (OR, 3.38 [95% CI, 1.98 to 5.77]; p < 0.001), and hypo-HDLemia (OR, 2.07 [95% CI, 1.30 to 3.29]; p = 0.002) were significantly associated with posterosuperior rotator cuff tears. The VIF, conditional index, and ORs with 95% CIs for all of the variables are summarized in Table V. The p value of the Hosmer-Lemeshow test was 0.775, indicating a good fit.
TABLE V.
Strengths of Associations Between Studied Variables and Posterosuperior Rotator Cuff Tear on Multivariable Analysis: Metabolic Syndrome Excluded*
| Studied Variable | OR (95% CI) | P Value |
| Age | 1.86 (1.47-2.35) | <0.001† |
| BMI (kg/m2) | 1.09 (1.02-1.18) | 0.019† |
| Dominant-side involvement | 2.04 (1.38-3.01) | <0.001† |
| Manual labor | 9.48 (5.13-17.51) | <0.001† |
| Diabetes | 3.38 (1.98-5.77) | <0.001† |
| Hypertension | 1.05 (0.68-1.62) | 0.824 |
| Ipsilateral carpal tunnel syndrome | 0.78 (0.50-1.22) | 0.276 |
| Hypo-HDLemia | 2.07 (1.30-3.29) | 0.002† |
The variance inflation factor (VIF) and the conditional index were 1.136 and 5.088, respectively; the p value of the Hosmer-Lemeshow test was 0.775.
Significant.
The second multivariable analysis included age, dominant-side involvement, manual labor, metabolic syndrome, and ipsilateral carpal tunnel syndrome. There was no multicollinearity among the 5 variables. Age (OR, 1.85 [95% CI, 1.48 to 2.31]; p < 0.001), dominant-side involvement (OR, 1.83 [95% CI, 1.26 to 2.67]; p = 0.002), manual labor (OR, 7.71 [95% CI, 4.33 to 13.73]; p < 0.001), and metabolic syndrome (OR, 1.98 [95% CI, 1.35 to 2.91]; p < 0.001) were significantly associated with posterosuperior rotator cuff tears. The VIF, conditional index, and ORs with 95% CIs for all of the variables are summarized in Table VI. The p value of the Hosmer-Lemeshow test was 0.615, indicating a good fit.
TABLE VI.
Strengths of Associations Between Studied Variables and Posterosuperior Rotator Cuff Tear on Multivariable Analysis: BMI, Diabetes, Hypertension, and Hypo-HDLemia Excluded*
| Studied Variable | OR (95% CI) | P Value |
| Age | 1.85 (1.48-2.31) | <0.001† |
| Dominant-side involvement | 1.83 (1.26-2.67) | 0.002† |
| Manual labor | 7.71 (4.33-13.73) | <0.001† |
| Metabolic syndrome | 1.98 (1.35-2.91) | <0.001† |
| Ipsilateral carpal tunnel syndrome | 0.88 (0.57-1.35) | 0.555 |
The variance inflation factor (VIF) and the conditional index were 1.093 and 4.563, respectively; the p value of the Hosmer-Lemeshow test was 0.615.
Significant.
Discussion
This study demonstrated that, in a general population from rural South Korea, atraumatic posterosuperior rotator cuff tears were significantly associated with age, dominant-side involvement, manual labor, diabetes, BMI, hypo-HDLemia, and metabolic syndrome. The ORs of these factors, with the exception of BMI, suggest substantial clinical relevance.
Previous studies indicated that the prevalence of posterosuperior rotator cuff tears increases with age and that age is a risk factor for posterosuperior rotator cuff tears2,25-34. Our study further establishes that age is an independent risk factor for a posterosuperior rotator cuff tear, supporting the consensus that an atraumatic posterosuperior rotator cuff tear is a result of the degenerative process that accompanies aging28,30.
Controversy exists as to whether a posterosuperior rotator cuff tear more commonly affects the dominant upper extremity. Milgrom et al. found no relation between hand dominance and asymptomatic rotator cuff tears30. Keener et al. reported that hand dominance is related to symptomatic rotator cuff tears, especially tears involving shoulder pain35. In the present study, which included participants with asymptomatic and symptomatic posterosuperior rotator cuff tears, we found atraumatic posterosuperior rotator cuff tears to be more prevalent in the dominant upper extremity34. In a general-population study similar to ours, Yamamoto et al. reported a similar association between posterosuperior rotator cuff tears and the dominant upper extremity2. Our finding that manual labor was significantly associated with posterosuperior rotator cuff tears is consistent with the expectation that the dominant upper extremity has greater exposure to repetitive and overuse activities.
The finding that the manual labor involved in agricultural work is significantly associated with posterosuperior rotator cuff tears is consistent with other epidemiologic studies indicating a high prevalence of rotator cuff tears among manual laborers, including agricultural workers3,27,36,37. Additionally, our results support those of previous biomechanical studies that suggested that manual labor activities, including sustained or repeated arm abduction, heavy lifting or carrying, high task repetitiveness, and physical exertion, are associated with posterosuperior rotator cuff tears36,38,39.
The finding that diabetes is strongly associated with posterosuperior rotator cuff tears is consistent with the findings of several previous studies noting diabetes as a risk factor for a rotator cuff tear and for a retear after rotator cuff repair26,34,40. It was recently reported that even plasma glucose levels at the high end of the normal range may be a risk factor for a rotator cuff tear9. Other authors reported a significant association between hyperglycemia and Achilles tendon tendinopathy and considered insulin resistance, an aspect of metabolic syndrome, as a possible cause41. Our study also found that metabolic syndrome, which is strongly related to insulin resistance and hyperglycemia13, was associated with posterosuperior rotator cuff tears. On the molecular level, hyperglycemia induces oxidative stress and cytokine production, which lead to inflammation and result in damage in various tissues42-45. Hyperglycemia alters collagen structure through a glycation process46,47 and also reduces proteoglycan levels through decreased synthesis or sulfation of glycosaminoglycans48. These molecular mechanisms may affect rotator cuff tendon degeneration.
Our finding of a significant association between BMI and posterosuperior rotator cuff tears is consistent with previous studies noting that both BMI and percentage of body fat are strongly associated with the prevalence and severity of rotator cuff tears6,8. One proposed mechanism of the effect of obesity on tendon degeneration is cellular inflammation through the disturbed production of adipokines in adipose tissue; decreased production of adiponectin and increased leptin resistance induce intracellular reactive oxygen species, which induce inflammation and apoptosis of cells49,50. In obesity, oxidative stress on tendons may be accelerated by increased proinflammatory cytokines, including plasminogen activator inhibitor, tumor necrosis factor (TNF)-α, angiotensinogen, and interleukins 6, 8, 10, and 1850. The present study did not evaluate an association between obesity and adipokines but did confirm that obesity, a factor of metabolic syndrome, is significantly associated with posterosuperior rotator cuff tears. However, the strength of association between BMI and a posterosuperior rotator cuff tear was low compared with that of the other studied metabolic parameters. Therefore, the clinical relevance of obesity may not be substantial.
The relationship between serum lipids and rotator cuff tears remains unclear7,8,51. In the current study, we found that hypo-HDLemia was significantly associated with posterosuperior rotator cuff tears. Abboud and Kim reported that serum levels of total cholesterol, TG, and LDL were higher and of HDL were lower among patients with a rotator cuff tear compared with a control group51. Djerbi et al. reported that the prevalence of rotator cuff tears was greater among patients with dyslipidemia7. Abate et al. reported that lower levels of HDL and higher levels of TG were significantly more prevalent among women with a rotator cuff tear8. However, Longo et al. reported no association between rotator cuff tears and either serum TG concentration or serum total cholesterol concentration12.
Metabolic syndrome is a well-known risk factor for various degenerative diseases, including cardiovascular disease, stroke, and diabetes as well as osteoarthritis and Achilles enthesopathy13,52-54. We found that metabolic syndrome was significantly associated with posterosuperior rotator cuff tears. The authors of a previous study reported metabolic syndrome as a possible risk factor for shoulder pain in men but were unable to demonstrate a significant association between metabolic syndrome and rotator cuff tears because rotator cuff integrity was not evaluated14. Our univariate analysis showed that a number of components of metabolic syndrome were significantly associated with posterosuperior rotator cuff tears. The associations between posterosuperior rotator cuff tears and several factors, including obesity, diabetes, and dyslipidemia, suggest a molecular link between posterosuperior rotator cuff tears and metabolic syndrome. This finding strongly suggests that metabolic syndrome is a risk factor for a posterosuperior rotator cuff tear, although the molecular mechanism and the pathophysiology of that association have not been determined.
This investigation had several limitations. Although this was a cohort study, we were only able to include subjects who volunteered, and they may not be representative of the entire population. Agricultural workers made up a major portion of this investigation’s population, and their characteristics may not be generalizable to populations in other locations. Because labor activity was significantly associated with posterosuperior rotator cuff tears, the rates of cuff tear may be higher in this cohort than in the general population. It is also possible that a dietary difference exists between this study’s cohort and an urban population and this could affect metabolic parameters. However, the American and European heart associations do not accept rural residence as a conventional cardiovascular risk factor55,56. Although this cross-sectional study did demonstrate a significant association between diabetes and posterosuperior rotator cuff tears and between hypo-HDLemia and posterosuperior rotator cuff tears, we could not evaluate the cumulative effects of serum lipid abnormalities on posterosuperior rotator cuff tears and any association between the duration or severity of diabetes and posterosuperior rotator cuff tears. We evaluated the association between labor and rotator cuff tears, but we did not evaluate according to the specific type of occupation or sports activity, or the cumulative effect of labor. While the importance of the significantly associated factors is not affected by these limitations, the relevance to other populations may be limited.
The present study also had strengths. Posterosuperior rotator cuff tears were diagnosed using MRI findings. In the previous general-population studies2,27, the existence of a rotator cuff tear was determined by ultrasound instead of MRI, which has higher interobserver reliability57. In addition, MRI findings are also more useful for diagnosing subscapularis tendon tears, so in the current study, we were able to exclude subscapularis tendon tears58. Lastly, the inclusion and study of a general population likely provides information about the pathogenesis of rotator cuff tears that is less biased than that of studies of cohorts with symptomatic rotator cuff tears.
In summary, the metabolic factors of diabetes, BMI, hypo-HDLemia, and metabolic syndrome were significant independent factors associated with the development of a posterosuperior rotator cuff tear.
Acknowledgments
Note: The authors express their gratitude to Sang-Il Lee, MD, PhD, and Ki Soo Park, MD, PhD, for their contributions to the securing of funding for this study. They also thank Hyun-su Yang, MS, who supported the statistical aspects of this project throughout the entire process.
Footnotes
Investigation performed at Gyeongsang National University Changwon Hospital, Changwon, and Gyeongsang National University Hospital, Jinju, Republic of Korea
Disclosure: This study was supported by a grant from the Farmers’ Musculoskeletal Disease Investigation of the Korean Rural Development Administration. The Disclosure of Potential Conflicts of Interest forms are provided with the online version of the article (http://links.lww.com/JBJS/E806).
References
- 1.Via AG, De Cupis M, Spoliti M, Oliva F. Clinical and biological aspects of rotator cuff tears. Muscles Ligaments Tendons J. 2013. July 9;3(2):70-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Yamamoto A, Takagishi K, Osawa T, Yanagawa T, Nakajima D, Shitara H, Kobayashi T. Prevalence and risk factors of a rotator cuff tear in the general population. J Shoulder Elbow Surg. 2010. January;19(1):116-20. [DOI] [PubMed] [Google Scholar]
- 3.Roquelaure Y, Ha C, Leclerc A, Touranchet A, Sauteron M, Melchior M, Imbernon E, Goldberg M. Epidemiologic surveillance of upper-extremity musculoskeletal disorders in the working population. Arthritis Rheum. 2006. October 15;55(5):765-78. [DOI] [PubMed] [Google Scholar]
- 4.Tashjian RZ, Granger EK, Farnham JM, Cannon-Albright LA, Teerlink CC. Genome-wide association study for rotator cuff tears identifies two significant single-nucleotide polymorphisms. J Shoulder Elbow Surg. 2016. February;25(2):174-9. Epub 2015 Sep 5. [DOI] [PubMed] [Google Scholar]
- 5.Wendelboe AM, Hegmann KT, Gren LH, Alder SC, White GL, Jr, Lyon JL. Associations between body-mass index and surgery for rotator cuff tendinitis. J Bone Joint Surg Am. 2004. April;86(4):743-7. [DOI] [PubMed] [Google Scholar]
- 6.Gumina S, Candela V, Passaretti D, Latino G, Venditto T, Mariani L, Santilli V. The association between body fat and rotator cuff tear: the influence on rotator cuff tear sizes. J Shoulder Elbow Surg. 2014. November;23(11):1669-74. Epub 2014 Jun 4. [DOI] [PubMed] [Google Scholar]
- 7.Djerbi I, Chammas M, Mirous MP, Lazerges C, Coulet B; French Society For Shoulder and Elbow (SOFEC). Impact of cardiovascular risk factor on the prevalence and severity of symptomatic full-thickness rotator cuff tears. Orthop Traumatol Surg Res. 2015. October;101(6)(Suppl):S269-73. Epub 2015 Aug 28. [DOI] [PubMed] [Google Scholar]
- 8.Abate M, Schiavone C, Di Carlo L, Salini V. Prevalence of and risk factors for asymptomatic rotator cuff tears in postmenopausal women. Menopause. 2014. March;21(3):275-80. [DOI] [PubMed] [Google Scholar]
- 9.Longo UG, Franceschi F, Ruzzini L, Spiezia F, Maffulli N, Denaro V. Higher fasting plasma glucose levels within the normoglycaemic range and rotator cuff tears. Br J Sports Med. 2009. April;43(4):284-7. Epub 2008 Sep 23. [DOI] [PubMed] [Google Scholar]
- 10.Oliva F, Osti L, Padulo J, Maffulli N. Epidemiology of the rotator cuff tears: a new incidence related to thyroid disease. Muscles Ligaments Tendons J. 2014. November 17;4(3):309-14. [PMC free article] [PubMed] [Google Scholar]
- 11.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. September;23(9):1282-8. Epub 2014 Mar 4. [DOI] [PubMed] [Google Scholar]
- 12.Longo UG, Franceschi F, Spiezia F, Forriol F, Maffulli N, Denaro V. Triglycerides and total serum cholesterol in rotator cuff tears: do they matter? Br J Sports Med. 2010. October;44(13):948-51. Epub 2009 Apr 8. [DOI] [PubMed] [Google Scholar]
- 13.Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet. 2005. April 16-22;365(9468):1415-28. [DOI] [PubMed] [Google Scholar]
- 14.Rechardt M, Shiri R, Karppinen J, Jula A, Heliövaara 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. July 20;11:165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Tuite MJ, Yandow DR, DeSmet AA, Orwin JF, Quintana FA. Diagnosis of partial and complete rotator cuff tears using combined gradient echo and spin echo imaging. Skeletal Radiol. 1994. October;23(7):541-5. [DOI] [PubMed] [Google Scholar]
- 16.Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL, Jr, Jones DW, Materson BJ, Oparil S, Wright JT, Jr, Roccella EJ; Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. National Heart, Lung, and Blood Institute; National High Blood Pressure Education Program Coordinating Committee. Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension. 2003. December;42(6):1206-52. Epub 2003 Dec 1. [DOI] [PubMed] [Google Scholar]
- 17.Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Jr, Spertus JA, Costa F; American Heart Association; National Heart, Lung, and Blood Institute. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005. October 25;112(17):2735-52. Epub 2005 Sep 12. [DOI] [PubMed] [Google Scholar]
- 18.Alberti KG, Zimmet P, Shaw J; IDF Epidemiology Task Force Consensus Group. The metabolic syndrome—a new worldwide definition. Lancet. 2005. September 24-30;366(9491):1059-62. [DOI] [PubMed] [Google Scholar]
- 19.Lee SY, Park HS, Kim DJ, Han JH, Kim SM, Cho GJ, Kim DY, Kwon HS, Kim SR, Lee CB, Oh SJ, Park CY, Yoo HJ. Appropriate waist circumference cutoff points for central obesity in Korean adults. Diabetes Res Clin Pract. 2007. January;75(1):72-80. Epub 2006 Jun 2. [DOI] [PubMed] [Google Scholar]
- 20.Jameson JL, Mandel SJ, Weetman AP. Disorders of the thyroid gland. In: Kasper DL, Fauci AS, Longo DL, Hauser SL, Jameson JL, Loscalzo J, editors. Harrison’s principles of internal medicine. 19th ed New York: McGraw-Hill; 2015. p 2283-308. [Google Scholar]
- 21.Cartwright MS, Yeboah S, Walker FO, Rosenbaum DA, Newman JC, Arcury TA, Mora DC, Quandt SA. Examining the association between musculoskeletal injuries and carpal tunnel syndrome in manual laborers. Muscle Nerve. 2016. June;54(1):31-5. Epub 2016 Jan 5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Johnson EW, Kukla RD, Wongsam PE, Piedmont A. Sensory latencies to the ring finger: normal values and relation to carpal tunnel syndrome. Arch Phys Med Rehabil. 1981. May;62(5):206-8. [PubMed] [Google Scholar]
- 23.Belsley DA. Regression diagnostics: identifying influential data and sources of collinearity. Hoboken: Wiley-Interscience; 2004. [Google Scholar]
- 24.Moosmayer S, Tariq R, Stiris M, Smith HJ. The natural history of asymptomatic rotator cuff tears: a three-year follow-up of fifty cases. J Bone Joint Surg Am. 2013. July 17;95(14):1249-55. [DOI] [PubMed] [Google Scholar]
- 25.Tempelhof S, Rupp S, Seil R. Age-related prevalence of rotator cuff tears in asymptomatic shoulders. J Shoulder Elbow Surg. 1999. Jul-Aug;8(4):296-9. [DOI] [PubMed] [Google Scholar]
- 26.Jeong J, Shin DC, Kim TH, Kim K. Prevalence of asymptomatic rotator cuff tear and their related factors in the Korean population. J Shoulder Elbow Surg. 2017. January;26(1):30-5. Epub 2016 Aug 3. [DOI] [PubMed] [Google Scholar]
- 27.Minagawa H, Yamamoto N, Abe H, Fukuda M, Seki N, Kikuchi K, Kijima H, Itoi E. Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: from mass-screening in one village. J Orthop. 2013. February 26;10(1):8-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Moosmayer S, Smith HJ, Tariq R, Larmo A. Prevalence and characteristics of asymptomatic tears of the rotator cuff: an ultrasonographic and clinical study. J Bone Joint Surg Br. 2009. February;91(2):196-200. [DOI] [PubMed] [Google Scholar]
- 29.Yamaguchi K, Ditsios K, Middleton WD, Hildebolt CF, Galatz LM, Teefey SA. The demographic and morphological features of rotator cuff disease. A comparison of asymptomatic and symptomatic shoulders. J Bone Joint Surg Am. 2006. August;88(8):1699-704. [DOI] [PubMed] [Google Scholar]
- 30.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. March;77(2):296-8. [PubMed] [Google Scholar]
- 31.Worland RL, Lee D, Orozco CG, SozaRex F, Keenan J. Correlation of age, acromial morphology, and rotator cuff tear pathology diagnosed by ultrasound in asymptomatic patients. J South Orthop Assoc. 2003. Spring;12(1):23-6. [PubMed] [Google Scholar]
- 32.Moor BK, Röthlisberger M, Müller DA, Zumstein MA, Bouaicha S, Ehlinger M, Gerber C. Age, trauma and the critical shoulder angle accurately predict supraspinatus tendon tears. Orthop Traumatol Surg Res. 2014. September;100(5):489-94. Epub 2014 Jul 8. [DOI] [PubMed] [Google Scholar]
- 33.Gumina S, Carbone S, Campagna V, Candela V, Sacchetti FM, Giannicola G. The impact of aging on rotator cuff tear size. Musculoskelet Surg. 2013. June;97(Suppl 1):69-72. Epub 2013 Apr 16. [DOI] [PubMed] [Google Scholar]
- 34.Abate M, Schiavone C, Salini V. Sonographic evaluation of the shoulder in asymptomatic elderly subjects with diabetes. BMC Musculoskelet Disord. 2010. December 7;11:278. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Keener JD, Steger-May K, Stobbs G, Yamaguchi K. Asymptomatic rotator cuff tears: patient demographics and baseline shoulder function. J Shoulder Elbow Surg. 2010. December;19(8):1191-8. Epub 2010 Oct 27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Seidler A, Bolm-Audorff U, Petereit-Haack G, Ball E, Klupp M, Krauss N, Elsner G. Work-related lesions of the supraspinatus tendon: a case-control study. Int Arch Occup Environ Health. 2011. April;84(4):425-33. Epub 2010 Aug 25. [DOI] [PubMed] [Google Scholar]
- 37.Rolf O, Ochs K, Böhm TD, Baumann B, Kirschner S, Gohlke F. [Rotator cuff tear—an occupational disease? An epidemiological analysis]. Z Orthop Ihre Grenzgeb. 2006. Sep-Oct;144(5):519-23. German. [DOI] [PubMed] [Google Scholar]
- 38.Bodin J, Ha C, Chastang JF, Descatha A, Leclerc A, Goldberg M, Imbernon E, Roquelaure Y. Comparison of risk factors for shoulder pain and rotator cuff syndrome in the working population. Am J Ind Med. 2012. July;55(7):605-15. Epub 2011 Dec 27. [DOI] [PubMed] [Google Scholar]
- 39.Svendsen SW, Gelineck J, Mathiassen SE, Bonde JP, Frich LH, Stengaard-Pedersen K, Egund N. Work above shoulder level and degenerative alterations of the rotator cuff tendons: a magnetic resonance imaging study. Arthritis Rheum. 2004. October;50(10):3314-22. [DOI] [PubMed] [Google Scholar]
- 40.Cho NS, Moon SC, Jeon JW, Rhee YG. The influence of diabetes mellitus on clinical and structural outcomes after arthroscopic rotator cuff repair. Am J Sports Med. 2015. April;43(4):991-7. Epub 2015 Jan 26. [DOI] [PubMed] [Google Scholar]
- 41.Gaida JE, Alfredson L, Kiss ZS, Wilson AM, Alfredson H, Cook JL. Dyslipidemia in Achilles tendinopathy is characteristic of insulin resistance. Med Sci Sports Exerc. 2009. June;41(6):1194-7. [DOI] [PubMed] [Google Scholar]
- 42.Baynes JW, Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes. 1999. January;48(1):1-9. [DOI] [PubMed] [Google Scholar]
- 43.Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, Ciotola M, Quagliaro L, Ceriello A, Giugliano D. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation. 2002. October 15;106(16):2067-72. [DOI] [PubMed] [Google Scholar]
- 44.Kowluru RA, Engerman RL, Kern TS. Diabetes-induced metabolic abnormalities in myocardium: effect of antioxidant therapy. Free Radic Res. 2000. January;32(1):67-74. [DOI] [PubMed] [Google Scholar]
- 45.Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000. April 13;404(6779):787-90. [DOI] [PubMed] [Google Scholar]
- 46.Reddy GK. Glucose-mediated in vitro glycation modulates biomechanical integrity of the soft tissues but not hard tissues. J Orthop Res. 2003. July;21(4):738-43. [DOI] [PubMed] [Google Scholar]
- 47.Reddy GK, Stehno-Bittel L, Enwemeka CS. Glycation-induced matrix stability in the rabbit Achilles tendon. Arch Biochem Biophys. 2002. March 15;399(2):174-80. [DOI] [PubMed] [Google Scholar]
- 48.Burner T, Gohr C, Mitton-Fitzgerald E, Rosenthal AK. Hyperglycemia reduces proteoglycan levels in tendons. Connect Tissue Res. 2012;53(6):535-41. Epub 2012 Aug 14. [DOI] [PubMed] [Google Scholar]
- 49.Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation. 2005. March 22;111(11):1448-54. [DOI] [PubMed] [Google Scholar]
- 50.Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011;29:415-45. [DOI] [PubMed] [Google Scholar]
- 51.Abboud JA, Kim JS. The effect of hypercholesterolemia on rotator cuff disease. Clin Orthop Relat Res. 2010. June;468(6):1493-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Wang H, Cheng Y, Shao D, Chen J, Sang Y, Gui T, Luo S, Li J, Chen C, Ye Y, Yang Y, Li Y, Zha Z. Metabolic syndrome increases the risk for knee osteoarthritis: a meta-analysis. Evid Based Complement Alternat Med. 2016;2016:7242478 Epub 2016 Oct 11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Li H, George DM, Jaarsma RL, Mao X. Metabolic syndrome and components exacerbate osteoarthritis symptoms of pain, depression and reduced knee function. Ann Transl Med. 2016. April;4(7):133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54.Abate M, Di Carlo L, Salini V, Schiavone C. Metabolic syndrome associated to non-inflammatory Achilles enthesopathy. Clin Rheumatol. 2014;33(10):1517-22. Epub 2014 Feb 19. [DOI] [PubMed] [Google Scholar]
- 55.MacDonald LA, Bertke S, Hein MJ, Judd S, Baron S, Merritt R, Howard VJ. Prevalence of cardiovascular health by occupation: a cross-sectional analysis among U.S. workers aged ≥45 years. Am J Prev Med. 2017. August;53(2):152-61. Epub 2017 Apr 11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Limdi NA, Howard VJ, Higginbotham J, Parton J, Safford MM, Howard G. US Mortality: influence of race, geography and cardiovascular risk among participants in the population-based REGARDS cohort. J Racial Ethn Health Disparities. 2016. December;3(4):599-607. Epub 2015 Nov 5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Okoroha KR, Mehran N, Duncan J, Washington T, Spiering T, Bey MJ, Van Holsbeeck M, Moutzouros V. Characterization of rotator cuff tears: ultrasound versus magnetic resonance imaging. Orthopedics. 2017. January 1;40(1):e124-30. Epub 2016 Oct 18. [DOI] [PubMed] [Google Scholar]
- 58.Martín-Hervás C, Romero J, Navas-Acién A, Reboiras JJ, Munuera L. Ultrasonographic and magnetic resonance images of rotator cuff lesions compared with arthroscopy or open surgery findings. J Shoulder Elbow Surg. 2001. Sep-Oct;10(5):410-5. [DOI] [PubMed] [Google Scholar]