Abstract
Background:
Although the function of vitamin D in bone metabolism has been well studied, the question remains whether vitamin D deficiency impairs tendon healing after rotator cuff repair.
Purpose:
To investigate the correlation between preoperative vitamin D deficiency and the retear rate and pain after arthroscopic rotator cuff repair.
Study Design:
Cohort study; Level of evidence, 3.
Methods:
Patients with full-thickness rotator cuff tears who underwent arthroscopic rotator cuff repair between January 2018 and August 2019 were enrolled. Included patients were divided into a control group (vitamin D level ≥20 μg/L) and a deficiency group (vitamin D level <20 μg/L). We investigated the association between preoperative vitamin D level and patient characteristics, MRI findings, pain and function scores (visual analog scale [VAS] for pain; Constant-Murley; University of California, Los Angeles; and American Shoulder and Elbow Surgeons scores), and healing status using the Pearson or Spearman correlation coefficient. The clinical characteristics were compared between the groups using the chi-square test or Fisher exact test.
Results:
Included were 89 patients (control group, 44 patients; deficiency group, 45 patients). The mean vitamin D levels were 25.07 ± 5.38 and 14.61 ± 3.43 μg/L in the control and deficiency groups, respectively (P < .001); otherwise, there were no significant differences between the groups in the variables under study. Vitamin D levels were not related to age, symptom duration, tear size, extent of retraction, VAS pain score preoperatively and at 6 and 24 months postoperatively, or any function scores. Supraspinatus fatty infiltration and VAS scores at 1 and 3 months postoperatively were significantly associated with vitamin D level (r = –0.360, –0.362, and –0.316, respectively; P < .05 for all). VAS scores were significantly lower in the control group than in the deficiency group at postoperative 1 month (1.09 ± 0.56 vs 1.47 ± 0.66, respectively) and 3 months (1.14 ± 0.77 vs 1.44 ± 0.66) (P < .05 for both). The retear rate was significantly lower in the control group than in the deficiency group (9.09% vs 26.67%, respectively; P < .05).
Conclusion:
Our study revealed that preoperative vitamin D deficiency was associated with a higher retear rate and early pain (1 and 3 months) after arthroscopic rotator cuff repair.
Keywords: vitamin D, rotator cuff, shoulder, arthroscopy, outcome
Rotator cuff tear is a common injury of the shoulder joint. According to an epidemiological survey of different age groups, the prevalence of rotator cuff injury in people older than 60 years is >25%. 38 Shoulder pain and dysfunction are the main clinical manifestations that seriously affect patients’ quality of life. At present, arthroscopic rotator cuff repair is the most effective strategy for treating full-thickness rotator cuff tears. Retear and pain after operation are the main concerns of patients. Many factors affect the outcomes after rotator cuff repair, including patient- and surgery-related factors, such as age, tear size, degree of fatty infiltration, smoking, presence of diabetes, osteoporosis, vitamin D levels, and suture technology. 1,23,29
Vitamin D deficiency is prevalent among patients who have undergone arthroscopic rotator cuff repair. 17,21,25,34 Vitamin D can regulate the metabolism of calcium and phosphorus, and it also participates in the regulation of cell proliferation and differentiation of the immune system. In addition to its role in bone growth and metabolism, the role of vitamin D in tendon healing after surgery has received increasing attention. 9,19 Experiments in mice have confirmed that vitamin D deficiency impairs early tendon healing after rotator cuff surgery, 2 and vitamin D supplementation can enhance postoperative tendon healing. 19
Despite the high prevalence of serum vitamin D deficiency among patients with rotator cuff tears, few studies have studied the vitamin D level in relation to rotator cuff healing and pain after repair. Therefore, this study aimed to evaluate the correlation between preoperative vitamin D deficiency and the retear rate and pain after arthroscopic rotator cuff repair. We hypothesized that preoperative vitamin D deficiency would be associated with a higher retear rate and early pain after arthroscopic rotator cuff repair.
Methods
Patient Selection
The protocol for this retrospective cohort study was approved by the hospital ethics committee, and informed consent was obtained from the study patients. Patients who underwent arthroscopic repair for a full-thickness rotator cuff tear between January 2018 and August 2019 were screened for this study. The inclusion criteria were as follows: (1) patients with full-thickness supraspinatus or supraspinatus/infraspinatus tears, in whom small- to large-sized tears (tear size <5 cm) were preoperatively diagnosed by magnetic resonance imaging (MRI); (2) patients in whom the preoperative serum vitamin D level (25-hydroxyvitamin D, μg/L) was tested; (3) patients aged ≥40 years and ≤75 years; and (4) patients with a body mass index (BMI) ≥18.5 and ≤30 kg/m2. The exclusion criteria were as follows: (1) patients who underwent single-row repair technique; (2) patients who had additional trauma or other shoulder diseases not related to the index surgery postoperatively; (3) patients who did not undergo MRI assessment of structural integrity at a minimum of 2 years postoperatively; and (4) patients who had received vitamin D supplementation postoperatively.
All patients had undergone serum vitamin D testing, computed tomography (CT) scan, and MRI scan before the operation. Measurement of the size of the rotator cuff tear was based on the maximum distance between the anterior and posterior edges of the tear in the oblique sagittal view of MRI scan 6 ; the retraction distance was based on the maximum distance between the medial and lateral edges of the tear in the oblique coronal view of MRI scan 8 ; and the degree of supraspinatus fatty infiltration was evaluated in the oblique sagittal view of the shoulder CT scan according to the Goutallier system. 12 According to previous criteria, 18 a serum vitamin D level <20 μg/L was diagnosed as vitamin D deficiency. Included patients were divided into 2 groups: the deficiency group (vitamin D level <20 μg/L) and the control group (vitamin D level ≥20 μg/L).
Surgical Procedures
All operations were completed by the same senior surgeon (G.X.) at our hospital with the patient under general anesthesia in the lateral decubitus position. Routine arthroscopic surgical procedures were performed, and the entire glenohumeral joint was explored. During operation, tenotomy or tenodesis was used for biceps lesions, and debridement was used for labral injuries without shoulder instability. After the glenohumeral joint lesions were treated, arthroscopy was transferred to the subacromial space to establish an anterolateral approach to perform acromion plasty and debridement to evaluate the size and repair tension of the rotator cuff tear. The footprint area was decortexed to prepare the bone bed. Then, an anchor (Johnson & Johnson or Linvatec Tech) was implanted at a suitable angle. The double-row repair technique was used in all patients included in the study.
Postoperative Pain Management and Rehabilitation
Nonsteroidal anti-inflammatory drugs (NSAIDs) as basic analgesics were used within 2 weeks after surgery, and opioid medication was added for untolerated pain. After that, NSAIDs and opioid medication were rarely prescribed.
According to rehabilitation guidelines, 37 the postoperative rehabilitation program was performed in stages. A progressive rehabilitation program was adopted for patients with small- and medium-sized tears, with local wrist and elbow joint activities in the first 3 weeks postoperatively, passive shoulder exercises at 3 to 6 weeks, and assisted shoulder activities from 6 weeks to 3 months. After 3 months, the patient could transition from partial resistance activities to normal sports activities. For large tears, we chose a delayed rehabilitation program. Passive shoulder joint activities were started 6 weeks postoperatively, active-assisted exercises were started 8 weeks later, and resistance exercises were performed 3 months later. However, the individual rehabilitation process was determined by the consensus of the surgeon, rehabilitation physician, and patient.
Evaluation of Clinical Outcomes
Each patient in the study was assessed preoperatively and at minimum 2-year follow-up. The following evaluations were used: visual analog scale (VAS) for pain score; University of California, Los Angeles (UCLA) score; 10 American Shoulder and Elbow Surgeons (ASES) score; 33 and Constant-Murley score. 7 In addition, the VAS score was assessed at 1 month, 3 months, and 6 months postoperatively.
The postoperative MRI scans were interpreted by a senior radiologist using a picture archiving and communications system workstation. The radiologist was blinded to each patient’s serum vitamin D level. Postoperative integrity of the rotator cuff structure was classified according to the Sugaya 36 system: type 1, sufficient thickness compared with a normal cuff with homogeneously low intensity on MRI scan; type 2, sufficient thickness compared with a normal cuff associated with a partial high-intensity area on MRI scan; type 3, insufficient thickness with less than half the thickness when compared with a normal cuff, but without discontinuity; type 4, the presence of a minor discontinuity on only 1 or 2 slices on oblique coronal and sagittal images; and type 5, a major discontinuity observed on >2 slices on both oblique coronal and sagittal images. Tears classified as types 4 and 5 were defined as retears.
Any complications or clinical failures were recorded. Joint infection was diagnosed when the patient reported a swollen joint, there was pus from the incision, and a microbial culture was positive. Anchor withdrawal was assessed according to radiological images. Revision surgery for any reason (eg, infection, stiffness, retear) was recorded.
Statistical Analysis
Normally distributed data were reported as mean ± standard deviation, and non-normally distributed variables were reported as median with interquartile range. A nonparametric test was used to analyze nonnormally distributed data. Count data were expressed as percentages, and they were compared between the groups using the chi-square test or Fisher exact test. Pearson or Spearman correlation coefficients were calculated for correlations between the vitamin D level and other variables. SPSS Version 22.0 software (IBM) was used to conduct the statistical analyses. A P value <.05 was regarded as statistically significant.
Results
Of an initial 135 patients, 89 patients were included in the study (Figure 1). There were 36 men and 53 women; their mean age was 61.20 ± 7.43 years, mean BMI was 23.55 ± 2.74 kg/m2, and mean symptom duration was 5.73 ± 7.70 months (Table 1). The mean vitamin D level was 19.78 ± 6.91 μg/L, and 45 patients were vitamin D deficient, accounting for about 50.56% of the study population (Table 1). All patients successfully underwent the operation and completed the follow-up. There were no serious complications in any patients.
Figure 1.
Study flowchart. MRI, magnetic resonance imaging.
Table 1.
Demographic and Clinical Characteristics of All Patients (N = 89) a
| Demographic Characteristics | Value | Clinical Characteristics | Value |
|---|---|---|---|
| Age, y | 61.20 ± 7.43 | Tear size, cm | 1.96 ± 0.86 |
| Sex, male/female, n | 36/53 | Degree of fatty infiltration (Goutallier stage) | 1.40 ± 0.96 |
| Body mass index, kg/m2 | 23.55 ± 2.74 | Extent of retraction, cm | 2.00 ± 0.94 |
| Traumatic injury, yes/no, n | 49/40 | Symptom duration, mo, median (IQR) | 2 (1-7.5) |
| Location, left/right, n | 25/64 | Serum vitamin D level (μg/L) | 19.78 ± 6.91 |
| Diabetic, n (%) | 9 (10.11) | Vitamin D deficiency, n (%) | 45 (50.56) |
| Smoker, n (%) | 19 (21.35) |
a Data are presented as mean ± SD unless otherwise indicated. IQR, interquartile range.
Correlations between vitamin D level and the other variables are shown in Table 2. Results indicated that BMI, degree of supraspinatus fatty infiltration, and VAS score at 1 month and 3 months postoperatively were correlated with vitamin D level (P < .05 for all).
Table 2.
Correlation of the Vitamin D Level With Other Variables a
| Variable | r | P Value |
|---|---|---|
| Age | –0.069 | .523 |
| Body mass index | –0.268 | .011 |
| Symptom duration | –0.050 | .645 |
| Tear size | –0.037 | .728 |
| Degree of fatty infiltration | –0.360 | .556 |
| Extent of retraction | 0.063 | .936 |
| VAS pain score | ||
| Preoperative | –0.030 | .781 |
| 1 mo postoperative | –0.362 | <.001 |
| 3 mo postoperative | –0.316 | .003 |
| 6 mo postoperative | –0.113 | .292 |
| 24 mo postoperative | –0.199 | .061 |
| UCLA score | ||
| Preoperative | 0.074 | .488 |
| Postoperative | –0.120 | .262 |
| Constant-Murley score | ||
| Preoperative | 0.021 | .844 |
| Postoperative | –0.175 | .101 |
| ASES score | ||
| Preoperative | –0.100 | .350 |
| Postoperative | –0.142 | .183 |
a Boldface P values indicate statistical significance (P < .05). ASES, American Shoulder and Elbow Surgeons; UCLA, University of California Los Angeles; VAS, visual analog scale.
There were 45 patients in the deficiency group and 44 patients in the control group. Table 3 shows the demographic and clinical characteristics of each group. Aside from vitamin D level, there were no significant differences between the groups.
Table 3.
Comparison of Demographic and Clinical Characteristics Between the Study Groups a
| Variable | Control Group (n = 44) |
Deficiency Group (n = 45) |
P Value |
|---|---|---|---|
| Age, y | 60.61 ± 7.62 | 61.78 ± 7.29 | .463 b |
| Sex, male/female, n | 19/25 | 17/28 | .604 c |
| Body mass index, kg/m2 | 23.15 ± 2.76 | 23.95 ± 2.70 | .171 b |
| Diabetic, n | 4 | 5 | .752 c |
| Smoker, n | 10 | 9 | .754 c |
| Traumatic injury, yes/no, n | 26/18 | 23/22 | .449 c |
| Location, left/right, n | 13/31 | 12/33 | .763 c |
| Symptom duration, mo | 6.09 ± 6.96 | 5.37 ± 8.41 | .055 d |
| Tear size, cm | 1.91 ± 0.87 | 2.00 ± 0.85 | .644 b |
| Degree of fatty infiltration (Goutallier stage) | 1.20 ± 0.93 | 1.60 ± 0.96 | .052 b |
| Goutallier stage >2, n | 3 | 6 | .308 c |
| Extent of retraction, cm | 1.95 ± 0.97 | 2.07 ± 0.90 | .549 b |
| No. of anchors | 2.80 ± 0.98 | 2.56 ± 0.66 | .180 b |
| Serum vitamin D level, μg/L | 25.07 ± 5.38 | 14.61 ± 3.43 | <.001 b |
a Data are reported as mean ± SD unless otherwise noted. Boldface P value indicates statistical significance (P < .05).
b Independent-samples t test.
c Chi-square test.
d Nonparametric test.
The preoperative and postoperative VAS pain scores in the control and deficiency groups are shown in Table 4. Compared with preoperative scores, VAS pain scores at all time points after the operation were significantly reduced in patients in both groups (P < .05 for all). The VAS score was significantly lower in the control group than in the deficiency group at 1 month and 3 months postoperatively (P < .05 for both). The mean preoperative and postoperative Constant-Murley, UCLA, and ASES scores of both groups are also shown in Table 4. We found no significant differences in the preoperative or postoperative Constant-Murley, UCLA, or ASES scores between the groups (Table 4).
Table 4.
Comparison of Pain and Functional Outcome Scores Between the Groups a
| Variable | Control Group (n = 44) |
Deficiency Group (n = 45) |
P Value |
|---|---|---|---|
| VAS pain score | |||
| Preoperative | 7.11 ± 0.84 | 7.13 ± 0.87 | .914 |
| 1 mo postoperative | 1.09 ± 0.56 | 1.47 ± 0.66 | .005 |
| 3 mo postoperative | 1.14 ± 0.77 | 1.44 ± 0.66 | .045 |
| 6 mo postoperative | 1.14 ± 0.80 | 1.20 ± 0.59 | .668 |
| 24 mo postoperative | 0.68 ± 0.64 | 0.87 ± 0.55 | .147 |
| UCLA score | |||
| Preoperative | 15.30 ± 2.98 | 14.64 ± 2.67 | .280 |
| Postoperative | 33.05 ± 1.12 | 33.16 ± 1.04 | .632 |
| Constant-Murley score | |||
| Preoperative | 47.43 ± 4.80 | 46.47 ± 4.31 | .321 |
| Postoperative | 85.07 ± 3.90 | 85.20 ± 4.14 | .877 |
| ASES score | |||
| Preoperative | 47.58 ± 4.16 | 48.30 ± 4.43 | .431 |
| Postoperative | 84.62 ± 5.37 | 85.96 ± 5.36 | .244 |
a Data are reported as mean ± SD. Boldface P values indicate statistical significance (P < .05). ASES, American Shoulder and Elbow Surgeons; UCLA, University of California–Los Angeles; VAS, visual analog scale.
The distribution of tear types and the retear rates for each group are shown in Table 5. We noted a significant difference in the retear rate between the groups (P < .05). In addition, although the preoperative VAS score was not correlated with type of retear, VAS scores at 1, 3, 6, and 24 months postoperatively were positively correlated with type of retear (P < .05 for all) (Table 6).
Table 5.
Comparison of Tear Type and Retear Rate at Final Follow-up Between the Groups
| Control Group (n = 44) |
Deficiency Group (n = 45) |
|
|---|---|---|
| Sugaya type, n | ||
| Type 1 | 20 | 7 |
| Type 2 | 11 | 13 |
| Type 3 | 9 | 13 |
| Type 4 a | 2 | 8 |
| Type 5 a | 2 | 4 |
| Retear rate, % | 9.09 | 26.67 |
| P | .031 b | |
a Defined as retear.
b Statistically significant difference (P < .05, χ2 test).
Table 6.
Correlation Between the Visual Analog Scale (VAS) Score and Types of Retear at Different Time Points a
| VAS Pain Score | r | P Value |
|---|---|---|
| Preoperative | –0.034 | .754 |
| 1 mo postoperative | 0.361 | .001 |
| 3 mo postoperative | 0.377 | <.001 |
| 6 mo postoperative | 0.395 | <.001 |
| 24 mo postoperative | 0.334 | .001 |
a Boldface P values indicate statistical significance (P < .05).
Discussion
This study is the first to describe VAS scores after arthroscopic repair in relation to the serum vitamin D level. After the operation (1 and 3 months), the pain score was negatively correlated with the vitamin D level (r = –0.362 and –0.316, respectively; P < .05). At 6 and 12 months postoperatively, the VAS scores were not correlated with the vitamin D level (r = –0.113 and –0.199, respectively; P > .05). After the operation, the deficiency group, when compared with the control group, had more severe early pain (1.47 ± 0.66 vs 1.09 ± 0.56, respectively, at 1 month; 1.44 ± 0.66 vs 1.14 ± 0.77 at 3 months; all P < .05) and a higher retear rate (26.67% vs 9.09%; P < .05). Based on the results of the correlation analysis, patients who have a higher Sugaya type postoperatively may have more pain than those who have a lower Sugaya type (r = 0.361, 0.377, 0.395, and 0.334 at 1, 3, 6, and 24 months, respectively; all P < .05). The shoulder function scores, including the Constant-Murley, UCLA, and ASES scores, were not correlated with the vitamin D level. As well, we found no significant differences in function scores between the groups. Our results showed that vitamin D deficiency was prevalent in patients undergoing rotator cuff repair, accounting for 50.56% of cases. Thus, vitamin D deficiency is an important concern for surgeons.
Vitamin D deficiency has become a global health problem. One billion people in the world have a vitamin D deficiency. 17,25 Vitamin D is a kind of steroid produced in the skin by sunlight and is converted into its active form by the hydroxylation process in the liver and kidneys. 25 Vitamin D can promote calcium absorption and regulate circulating calcium and phosphate levels for normal bone mineralization by the vitamin D receptor. 17 In addition, vitamin D plays an important role in decreasing the inflammatory response by reducing proinflammatory cytokines 3 and promoting protein synthesis and skeletal muscle growth. 9
Although the correlation between pain and the vitamin D level has been previously investigated under other conditions, this is the first time the relationship between pain and vitamin D level has been reported in patients undergoing arthroscopic cuff repair. This study found that preoperative vitamin D deficiency was associated with early pain after rotator cuff repair. Low vitamin D levels have been reported to be associated with increased pain in observational studies. 16 The mechanisms for vitamin D in pain management are the anti-inflammatory effects mediated by reduced cytokine and prostaglandin release and effects on T-cell responses. 14,24 In vitro studies 25 have shown that vitamin D inhibits the synthesis of prostaglandin E2 (PGE2), which is an essential factor in inflammatory pain. 13 A clinical study 11 found that vitamin D supplementation can reduce musculoskeletal pain with decreased levels of inflammatory cytokines, including PGE2. Thereby, vitamin D plays a vital role in the presence of pain after arthroscopic rotator cuff repair, and vitamin D supplementation may reduce the VAS score of patients who have vitamin D deficiency. However, more randomized, placebo-controlled studies are needed before any conclusions can be drawn.
The correlations between the serum vitamin D level and rotator cuff tear features may be controversial. In 2009, Oh et al 30 investigated the vitamin D levels of 366 patients with rotator cuff injuries and found that vitamin D levels was correlated with fat infiltration of the rotator cuff tissue. This result was consistent with the present study’s finding, although the correlation coefficients of both studies were too low (<0.3) to suggest clinical significance. In 2015, Ryu et al 34 conducted a cohort study (91 cases) and found that low vitamin D levels were not correlated with the tear size, the extent of retraction, or degree of fatty infiltration in rotator cuff muscles. These different results may have been caused by the research conditions. Unlike the study by Ryu et al, our study excluded massive tears and only assessed the degree of supraspinatus fatty infiltration, which may have reduced statistical errors. The number of cases with a high degree of fatty infiltration (Goutallier stage >2) accounted for a very small percentage of cases in previous studies, 30,34 which may have limited the accuracy of correlation analysis.
The bone-tendon healing process after surgery is very complicated, as it involves many factors, including endogenous cells, cytokines, growth factors, and collagen fibers. The normal rotator cuff tendon footprint area contains 4 layers of structures: the tendon, unmineralized fibrocartilage, mineralized fibrocartilage, and bone tissue. After arthroscopic repair, these structures disappear and are replaced with fibrovascular scar tissue. Vitamin D can induce an increase in the content of type 1 collagen fibers and decrease type 3 collagen fibers, making the healing tendon similar to its original structure. 35 Some animal studies found that by blocking matrix metalloproteinases (MMPs), which can inhibit rotator cuff healing, vitamin D can promote the accumulation of fibrocartilage and collagen and improve tendon healing. 4,5
The effects of vitamin D deficiency on the retear rate after arthroscopic rotator cuff repair are still unclear. Some animal experiments confirmed that a sufficient vitamin D level promoted tendon-bone healing after rotator cuff repair. 2 Vitamin D can also inhibit MMPs and promote tendon healing. 4,5,9 In in vitro experiments, Bahar-Shany et al 3 found that vitamin D can block the expression of MMPs by inhibiting extracellular signal-regulated kinase, c-Jun N-terminal kinase, and the nuclear factor–κB pathway and promote tendon-bone healing. Vitamin D can also inhibit inflammatory factors, such as tumor necrosis factor α, interleukin 6, and C-reactive protein, to reduce local and systemic inflammatory reactions and relieve postoperative pain. 20 O’Donnell et al 29 analyzed 41,467 patients undergoing rotator cuff repair and found that vitamin D deficiency was significantly related to shoulder revision surgery. Harada et al 15 conducted database research and found that low preoperative vitamin D levels were significantly associated with complications after rotator cuff repair. Ryu et al 34 found that low vitamin D levels were not correlated with retear after arthroscopic rotator cuff repair; however, that study had a shortcoming in that 88% of the patients had vitamin D deficiency. To determine the relationships between serum vitamin D level (sufficiency vs deficiency) and healing status after repair, a certain number of patients with sufficient vitamin D levels are required, which may affect the accuracy of the results. Our result further confirmed that vitamin D deficiency was related to the retear rate after arthroscopic rotator cuff repair.
The treatment of rotator cuff tears has undergone many innovations in the past 30 years, 26,31,32 including surgical techniques, tissue engineering, and biological factors. However, because of the insufficient blood supply of the rotator cuff tissue, scar tissue is the main structure at the tendon-bone healing site after repair. 28 The retear rates after arthroscopic cuff repair are still not low. 22,27,36 Vitamin D as a biological factor may play an increasingly more critical role in the future.
Limitations
Several limitations of the present study should be mentioned. First, it was a retrospective cohort study, the sample size was small, and the level of evidence was low. Second, we did not assess some of the factors that can affect tendon-bone healing, such as the degree of overuse, osteoporosis, and sports activities. Third, only the preoperative serum vitamin D level was measured. The vitamin D level may fluctuate during follow-up after surgery. Thus, more clinical and basic studies are needed to identify the relationship between the vitamin D level and rotator cuff diseases.
Conclusion
Our study revealed that preoperative vitamin D deficiency was associated with a higher retear rate and early pain after arthroscopic rotator cuff repair.
Footnotes
Final revision submitted August 2, 2022; accepted August 7, 2022.
The authors have declared that there are no conflicts of interest in the authorship and publication of this contribution. AOSSM checks author disclosures against the Open Payments Database (OPD). AOSSM has not conducted an independent investigation on the OPD and disclaims any liability or responsibility relating thereto.
Ethical approval for this study was obtained from Dongyang People’s Hospital (ref No. 2019-YX-057).
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