Abstract
Background
Although rotator cuff tears are one the most common musculoskeletal sources of disability, healing after rotator cuff repair (RCR) fails in >25% of cases. Existing data suggest that estradiol deficiency may be associated with worse postoperative outcomes following RCR. Thus, the purpose of this study was to determine whether estradiol supplementation among postmenopausal women is associated with better outcomes after RCR and we hypothesized that such an association would exist.
Methods
A retrospective review of all patients who underwent RCR by the lead author was done to identify those who were female and ≥50 years old, thus presumed to be postmenopausal. For all patients, all medications were recorded the day of surgery by the anesthesiologist in the preanesthesia note. These notes were reviewed to determine which patients were taking hormone replacement therapy (ie. “HRT”) and those who were not (i.e. “non-HRT) at the time of surgery. All patients were contacted at 2 years postoperatively. Subjective Shoulder Value (SSV), visual analog scale (VAS) for pain, and American Shoulder and Elbow Surgeons (ASES) score were collected, in addition to satisfaction and need for further reoperation.
Results
Overall, 254 women underwent RCR, of whom 2-year outcomes were obtained in 184 (74%) of which 42 (23%) were on estradiol supplementation at the time of surgery. There were no differences between groups in preoperative SSV (43 ± 21 non-HRT vs. 38 ± 22 HRT, P = .209), VAS (5.6 ± 2.3 vs. 5.7 ± 2.3, P = .770), or ASES scores (46 ± 20 vs. 44 ± 19, P = .738). However, HRT postmenopausal patients had significantly better VAS (1.2 ± 2.1 vs. 0.3 ± 0.8, P < .001) and SSV scores (87 ± 16 vs. 95 ± 10, P = .003) at 2-years postoperatively when compared to non-HRT postmenopausal patients. There were no significant differences in satisfaction (96.3% vs. 90.3%, P = .605), ASES scores (87 ± 17 vs. 94 ± 11, P = .146), or reoperation rates (7.9% vs. 14.8%, P = .297).
Conclusion
Estradiol supplementation was associated with better outcomes in postmenopausal women undergoing RCR; however, these differences in VAS and SSV did not meet the minimal clinically important threshold. Future prospective randomized studies could be considered before prescribing estradiol to postmenopausal patients in the setting of RCR.
Keywords: Rotator cuff repair, Rotator cuff tear, Estradiol, Hormone supplementation, Menopause, Patient-reported outcomes
Rotator cuff tears (RCTs) are a common musculoskeletal complaint, with a prevalence of anywhere from 5-40%, and have been noted to be more common in postmenopausal women.1,2,19 This is likely related to decreased estrogen production, as female patients with estrogen deficiency have been found to have 48% higher rates of RCT than those with normal estrogen levels,16 possibly due to more fragile tendons.9 One proposed mechanism relates to the positive relationship between estrogen and collagen synthesis. Estrogen is also involved in soft tissue laxity, which could result in stiffer rotator cuffs in estrogen-deficient states that are more prone to tearing than stretch.3 Older age, loss of muscle mass, and osteoporosis have also been implicated as contributing to higher rates of RCTs in postmenopausal women, and there is a clear relationship between osteoporosis and estrogen.5
Often, RCTs can be managed with a trial of nonoperative management. When these modalities—physical therapy, anti-inflammatories, activity modification, and steroid injections—fail to provide meaningful pain relief or restoration of function, rotator cuff repair (RCR) can be considered. RCR failure for the general population is estimated to range from 11-79%.11 However, as with the prevalence of RCTs, so is RCR failure more likely in women, making it important to identify modifiable factors for improving outcomes in this population.4
Postmenopausal women experience a decline in several sex hormones, of which estrogen is the most commonly used in hormone replacement therapy (HRT).14 These sex hormones have several proposed influences on the biomechanical properties of rotator cuff tendons. On a cellular level, in vitro studies on tendon cell lines have shown female sex hormones can increase cell proliferation.13 From a proteomic expression standpoint, the addition of estrogen-like compound to non–estrogen-deficient mice increased expression of osteogenic, angiogenic, and tendon maturation proteins.21 In mice tendons, “relatively immature granulation tissue was observed in the [estrogen deficient] group compared with the control group” and conversely, “the amount of chondroid tissue was greater and collagen organization was better in the control group than in the [estrogen deficient] group”.18 Postoperative estrogen supplementation in mice improved the structure of the healed rotator cuff tendon insertion, decreased inflammation, as well as improved growth and repair through the wingless Int-1, platelet derived growth factor, and transforming growth factor beta pathways.22 Similarly, combined raloxifene, an estrogen modulator, and vitamin-D supplementation prevented bone mineral density loss and improved healing of the tendon insertion in murine rotator cuff surgery.7
Despite the wealth of basic science research into the correlation of hormones and rotator cuff pathology, and previous findings of increased incidence of RCR surgery in estrogen-deficient females,16 to our knowledge there is limited clinical data connecting HRT and RCR outcomes. We hypothesized that, among postmenopausal women, estradiol supplementation would be associated with better postoperative patient-reported outcomes than controls.
Methods
This was a retrospective study on all female patients ≥50 years old who underwent RCR by the senior author at a single institution from 2017 to 2023. Demographic variables including age, body mass index (BMI), hand dominance, and occupation involving manual labor were collected. Patient-reported outcomes including the Subjective Shoulder Value (SSV), visual analog scale (VAS) for pain, and American Shoulder and Elbow Surgeons (ASES) score were collected preoperatively and postoperatively at 2 years. At the time of surgery, active medications, including any HRT, were recorded by the anesthesiologist and documented in their preoperative notes. These were used to establish the 2 patient cohorts: those on HRT (ie “HRT”) and those who were not (ie “non-HRT”). Notes were then reviewed to determine if the patients were taking either systemic estradiol or high-dose vaginal estradiol at the time of surgery. Vaginal estrogen over 0.025 mg/day was considered equivalent to systemic estradiol treatment, and grouped together as a high dose HRT category.15 The preoperative magnetic resonance imaging (MRI) was assessed to determine the rotator cuff tear width, degree of tearing (eg. partial vs. full) and amount of retraction. Intraoperatively, the presence of chondral damage, tendon delamination, axillary pouch osteophytes, coracoacromial ligament fraying and labrum and biceps pathology were recorded as binary variables. Superior labral anterior-posterior tears, humerus cartilage, and glenoid cartilage were all graded, and the acromial undersurface was assessed for small, medium, or large osteophytes. Each of the 4 rotator cuff tendons were graded on the Goutallier grading and the overall tendon quality and tendon loss was assessed as previously described.17 Following surgery, satisfaction and reoperation were recorded as binary variables.
Independent t-tests were conducted for continuous variables and chi-squared tests used to assess categorical variables. All statistics were computed using Stata (Stata Statistical Software; STATACorp, College Station, TX, USA).
Results
There were 254 female patients ≥50 years old identified with an average age of 61.8 years (range: 50-79). Of the 254 patients, 184 patients (74%) completed 2-year follow-up, of which 146 (79%) were on HRT at the time of surgery and 38 (21%) were not. There was no significant difference between non-HRT and HRT patients with regards to age (61.3 ± 7.0 years vs. 63.5 ± 1.5 years, P = .066), BMI (30.8 ± 6.9 kg/m2 vs. 28.6 ± 5.6 kg/m2, P = .071), hand dominance (P = .603), occupation (P = .719, Table I). There were no statistically significant differences in SSV, VAS, or ASES (P = .209, P = .770, and P = .738, respectively) preoperatively. There were no statistically significant differences in rotator cuff tear pattern, tear size, intraoperative findings (Table II).
Table I.
Demographics of non-HRT and HRT patients.
| Variable | HRT untreated | HRT value | P value |
|---|---|---|---|
| Age | 61.3 ± 7.0 | 63.5 ± 1.5 | .066 |
| BMI | 30.8 ± 6.9 | 28.6 ± 5.6 | .071 |
| Hand dominance (R) | 93.80% | 97.10% | .603 |
| Manual laborer | 3.90% | 2.70% | .719 |
HRT, hormone replacement therapy; BMI, body mass index.
Overall, 213 patients were not treated with HRT and 42 patients were treated with HRT. Averages and standard deviations for age and BMI for each of the 2 groups are shown. The percentage of patients in each of the 2 groups who are right hand–dominant and occupied as a manual laborer are shown.
Table II.
Intraoperative findings for non-HRT and HRT patients.
| Variable | N% | Untreated HRT | Treated HRT | P value |
|---|---|---|---|---|
| Tear retraction (mm) | 164 (89%) | 1.2 ± 1.0 | 1.2 ± 1.0 | .678 |
| Tear width (mm) | 164 (89%) | 2.0 ± 1.1 | 2.2 ± 1.1 | .455 |
| Humerus cartilage affected (%) | 158 (86%) | 7.3 ± 18.0 | 3.3 ± 10.9 | .209 |
| Glenoid cartilage affected (%) | 158 (86%) | 4.7 ± 13.3 | 2.8 ± 8.6 | .425 |
| Normal labrum | 155 (84%) | 83% | 86% | .756 |
| Normal biceps | 143 (78%) | 5% | 10% | .335 |
| Chondral damage | 126 (68%) | 21% | 17% | .693 |
| Tendon delamination | 169 (92%) | 10% | 16% | .311 |
| Infraspinatus/supraspinatus full-thickness tear | 145 (79%) | 62% | 63% | .887 |
| Subscapularis full-thickness tear | 143 (78%) | 14% | 17% | .697 |
| SLAP tear present | 39 (21%) | 75% | 88% | .453 |
| Supraspinatus Goutallier grade 0-1 | 158 (86%) | 81% | 69% | .126 |
| Infraspinatus Goutalliier grade 0-1 | 158 (86%) | 87% | 92% | .464 |
| Teres minor Goutallier grade 0-1 | 158 (86%) | 96% | 100% | .238 |
| Subscapularis Goutallier grade 0-1 | 158 (86%) | 95% | 97% | .533 |
| Tendon quality | .175 | |||
| Good | 82% | 76% | ||
| Fair | 14% | 14% | ||
| Poor | 3% | 11% | ||
| Tendon loss | .422 | |||
| None | 5% | 3% | ||
| Minimal | 85% | 81% | ||
| Substantial | 10% | 16% |
HRT, hormone replacement therapy; SLAP, superior labral anterior-posterior.
There were no differences in any finding. Averages and standard deviations for tear retraction, tear width, percent of affected humerus and glenoid cartilage are shown. The percentage of patients in each group with normal labrum, normal biceps, chondral damage, tendon delamination and SLAP tears as well as rotator cuff characteristics is shown.
With regards to postoperative outcomes, SSV was statistically significantly higher in the treated group after 2 years (87 ± 16 vs. 95 ± 10, P = .003). VAS after 2 years was higher in the non-HRT group (1.2 ± 2.1 vs. 0.3 ± 0.8, P < .001). While statistically significant, neither of these differences met the minimal clinically important difference for these measurements.6,20 There were no significant differences in ASES scores after 2 years (87 ± 17 vs. 94 ± 11, P = .146), satisfaction (P = .297), need for reoperation (P = .605), or evidence of MRI healing (P = .848) (Table III). Reoperation occurred in 11 patients. Five of 8 non-HRT patients and 2 of 3 HRT patients were treated with a single revision RCR. The remaining 3 non-HRT underwent reverse total shoulder arthroplasty. One HRT patient required 2 revision RCRs, a reverse total shoulder arthroplasty, as well as a revision arthroplasty when the initial revision failed.
Table III.
Outcomes for non-HRT and HRT patients.
| Variable | N (%) assessed | HRT untreated | HRT treated | P value |
|---|---|---|---|---|
| PreSSV | 160 (87%) | 43 ± 21 | 38 ± 22 | .209 |
| Pre-VAS | 162 (88%) | 5.6 ± 2.3 | 5.7 ± 2.3 | .77 |
| Pre-ASES | 142 (77%) | 46 ± 20 | 44 ± 19 | .738 |
| 2-yr SSV | 113 (61%) | 87 ± 16 | 95 ± 10 | .003 |
| 2-yr VAS | 120 (65%) | 1.2 ± 2.1 | 0.3 ± 0.8 | <.001 |
| 2-yr ASES | 65 (35%) | 87 ± 17 | 94 ± 11 | .146 |
| Satisfied | 151 (82%) | 90.30% | 96.30% | .605 |
| Reoperation Needed | 161 (88%) | 7.90% | 14.80% | .297 |
| Healed MRI | 28 (15%) | 64.70% | 60.00% | .848 |
HRT, hormone replacement therapy; SSV, Subjective Shoulder Value; VAS, visual analog scale; ASES, American Shoulder and Elbow Surgeons.
All patient-reported outcome scores improved with surgery for both groups. 2-year SSV and VAS differed between patients not treated and treated with HRT, with patients treated having significantly better outcomes. There was no difference in satisfaction or need for reoperation.
Discussion
In this study, postmenopausal patients treated with HRT were found to have statistically significant better SSV and VAS scores at 2 years postoperatively following RCR compared to patients who were not treated. ASES scores were not significantly different, and there were no statistically significant differences in reoperation rates in the 2 groups.
VAS, SSV, and reoperation rates were evaluated to show the effects of estradiol supplementation on RCR recovery; however, it is important to note that these measures are not direct reflections of retear rate or tendon healing. Postoperative imaging could elucidate if estradiol is improving the tendon healing itself, but without direct visual confirmation of the success of RCR, it is possible estradiol is working through other mechanisms besides direct tendon strengthening. It is possible HRT may contribute to clinical differences in patient recovery through its effect on bone and muscle. Future studies could determine whether postoperative failure at the bone–tendon interface, as compared to the musculotendinous interface, is influenced by estrogen treatment. HRT is also associated with increased muscle mass, which could mask the lack of difference in tendon healing between those treated and not treated with HRT.3 Patients treated with HRT may experience less atrophy and better muscle recovery, even if their repair fails, which may contribute to the differences in outcomes noted presently. Future studies could be aimed at better elucidation of the mechanism of action of estradiol to fully explain the differences in outcomes.
Beyond the direct effects of HRT on the rotator cuff, it is also plausible to consider that HRT could have an independent impact on patient-reported outcomes. Up to 70% of postmenopausal patients experience a musculoskeletal syndrome that includes worsening of arthritis and arthralgias.10 HRT has been shown to improve these symptoms independently from direct action on tendon, bone, or muscle, and could thus be contributing to the improvement of patient-reported outcomes in those treated with HRT.12 Additionally, providing validation to postmenopausal women that their symptoms can be explained in part by the musculoskeletal symptoms of menopause and addressing these symptoms with HRT can have a beneficial psychological impact, especially as it improves sleep, which is a major shared complaint among both cuff pathology and menopause.23 It is therefore possible that HRT is helping with psychological management of symptoms.
To our knowledge, this study is the first to evaluate the outcomes associated with HRT in RCR. Regardless of whether HRT is increasing the tendon or bone strength, improving only symptoms of retearing, increasing the effectiveness of physical therapy, or acting more in a psychological fashion, this study suggests improved clinical results following RCR in patients treated with HRT. Although the differences in the 2-year ASES scores between non-HRT and HRT were not statistically significant, and neither the 2-year SSV nor VAS was above the minimal clinical difference, there may be a role for HRT in improving clinical results. This study suggests that future randomized clinical trials should be considered as this could be a modifiable risk factor for failure.
There are several limitations to this study that warrant acknowledgement. First, this is a retrospective study of a single surgeon's practice at a single institution, thereby limiting its generalizability. Additional larger-scaled investigations are needed to assess the applicability of the present findings to the population at large. Second, it was not routine practice to obtain postoperative MRIs to assess for retear and therefore true differences in rates of this complication cannot be extrapolated from the present findings. Future investigations interested in answering this question would require postoperative MRIs. Third, it is important to note that the medical complications from HRT, such as thromboembolic sequelae, cannot be assessed in the study of this size due to their relative scarcity. Finally, patient estradiol levels were assumed based on menopausal status by age, rather than documented menopause or measured estradiol levels. Thus, it is possible some patients were assumed to have low levels of estradiol that related to their RCR recovery, when they in fact did not. While the cut-off for estradiol dosing was based on previous literature, there is disagreement as to which dose should be considered systemic, so while some patients were evaluated as treated with HRT, it is possible this HRT was not sufficient to affect tendon quality, and could explain poorer outcomes for these patients than others on higher doses.8,15 Moreover, whether a patient was treated with HRT was assessed by chart review, and thus patient compliance is in question, as well as if the patients were put on or remained on HRT during follow-up.
Conclusion
Estradiol supplementation associates with better outcomes in postmenopausal women undergoing RCR. Future prospective randomized studies could be considered before prescribing estradiol to postmenopausal patients in the setting of RCR.
Disclaimers:
Funding: No funding was disclosed by the authors.
Conflicts of interest: Christopher D. Joyce is a paid consultant for Zimmer Biomet and Enovis. Robert Z. Tashjian is a paid consultant for Zimmer Biomet, Enovis, and Stryker; has stock in Conextions and Genesis; receives intellectual property royalties from Zimmer Biomet, Stryker, and Shoulder Innovations; receives publishing royalties from Springer and the Journal of Bone and Joint Surgery; and serves on the editorial board of the Journal of Bone and Joint Surgery. Peter N. Chalmers is a paid consultant for DePuy, Smith + Nephew, Responsive Arthroscopy, and Exactech; receives intellectual property royalties from DePuy, Responsive Arthroscopy, and Exactech; has stock in TitinKM Biomedical; receives research support from DePuy, Smith + Nephew, and the National Institutes of Health; and serves on the editorial board of the Journal of Shoulder and Elbow Surgery. The other authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
Given his role as Editor in Chief, Dr. Peter N. Chalmers had no involvement in the peer-review of this article and has no access to information regarding its peer-review. Full responsibility for the editorial process for this article was delegated to Dr. John W. Sperling.
Footnotes
This research was approved by the University of Utah Institutional Review Board, IRB # 71740.
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