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Relationship between hematoma-like tissue on the footprint and structural outcome of arthroscopic rotator cuff repair with a transosseous technique

Open AccessPublished:January 13, 2023DOI:https://doi.org/10.1016/j.jseint.2022.12.019

      Abstract

      Background

      We have tried to create hematoma over the footprint site at the end of arthroscopic rotator cuff repair (ARCR) surgery, expecting to apply biochemical effects of the platelet-related factors. The purpose of this study was to investigate the presence of hematoma-like tissue (HLT) on postoperative MRI, and to evaluate the relationship between the HLT and the structural outcomes of ARCR.

      Materials & Methods

      Twenty-five patients were reviewed with a mean age at surgery of 69.8 years (range, 52–85 years). Postoperative MRI was performed at 1 week, 6–8 weeks, and >6 months postoperatively. Structural outcomes for the repaired cuff and thickness of HLT were evaluated on coronal T2-weighted images. Signal intensity of HLT was evaluated on coronal T2-weighted fat-suppressed images as the ratio compared to supraspinatus tendon intensity (HLT/SSP ratio).

      Results

      Structural outcomes showed Sugaya type 1 in 12 shoulders, type 2 in 4, and type 3 in 9. HLT thickness was significantly thicker at 1 week and 6–8 weeks postoperatively in Sugaya type 1 patients than in type 3 patients (1 week; p=.014, 6-8 weeks; p<.001). HLT/SSP ratio gradually decreased (at 1 week; 1.9±0.7, 6–8 weeks; 1.6±0.6, >6 months; 1.2±0.5), and differed significantly between >6 months and both 1 week and 6–8 weeks (p<.001 each).

      Conclusion

      Cases with thicker HLT at 1 week and 6-8 weeks postoperatively can expect good structural outcomes at >6 months. Signal intensity of the HLT became close to that of the supraspinatus tendon over time.

      Keywords

      In arthroscopic rotator cuff repair (ARCR), many reports have described attempts to decrease the retear rate using various modifications to repair methods
      • Bedeir Y.H.
      • Schumaier A.P.
      • Sheasha G.A.
      • Grawe B.M.
      Type 2 retear after arthroscopic single-row, double-row and suture bridge rotator cuff repair: a systematic review.
      , suture tension
      • Davidson P.A.
      • Rivenburgh D.W.
      Rotator cuff repair tension as a determinant of functional outcome.
      ,
      • Park S.G.
      • Shim B.J.
      • Seok H.G.
      How Much Will High Tension Adversely Affect Rotator Cuff Repair Integrity?.
      , and timing of the start of passive range-of-motion (ROM) exercises in rehabilitation
      • Houck D.A.
      • Kraeutler M.J.
      • Schuette H.B.
      • McCarty E.C.
      • Bravman J.T.
      Early Versus Delayed Motion After Rotator Cuff Repair: A Systematic Review of Overlapping Meta-analyses.
      .
      As another potential factor, the effect of hematoma including platelet-related factors on tendon-bone healing has been reported in association with the shoulder joint
      • Gumina S.
      • Campagna V.
      • Ferrazza G.
      • Giannicola G.
      • Fratalocchi F.
      • Milani A.
      • et al.
      Use of plateletleukocyte membrane in arthroscopic repair of large rotator cuff tears: A prospective randomized study.
      ,
      • Kobayashi M.
      • Itoi E.
      • Minagawa H.
      • Miyakoshi N.
      • Takahashi S.
      • Tuoheti Y.
      • et al.
      Expression of growth factors in the early phase of supraspinatus tendon healing in rabbits.
      . Platelet-derived growth factor has been shown to increase the early tensile strength of rotator cuff repairs in sheep models
      • Kobayashi M.
      • Itoi E.
      • Minagawa H.
      • Miyakoshi N.
      • Takahashi S.
      • Tuoheti Y.
      • et al.
      Expression of growth factors in the early phase of supraspinatus tendon healing in rabbits.
      . Use of the platelet-leukocyte membrane in the treatment of rotator cuff tears improved repair integrity compared with repair without the membrane
      • Gumina S.
      • Campagna V.
      • Ferrazza G.
      • Giannicola G.
      • Fratalocchi F.
      • Milani A.
      • et al.
      Use of plateletleukocyte membrane in arthroscopic repair of large rotator cuff tears: A prospective randomized study.
      .
      The Surface-Holding (SH) method, a modified transosseous-equivalent procedure using medial anchors and lateral transosseous sutures, has been reported to yield good results
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Araki N.
      • Chosa E.
      Surface-Holding Repair: An Original Arthroscopic Rotator Cuff Repair Technique.
      ,
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Yamaguchi H.
      • Inoue K.
      • et al.
      Bone marrow stimulation at the footprint of arthroscopic surface-holding repair advances cuff repair integrity.
      . In the SH method, induced mesenchymal stem cells from the portion of decortication allow the potential for differentiation into tendon tissues
      • Caplan A.I.
      Why are MSCs therapeutic? New data: new insight.
      and accelerate early remodeling during tendon-bone healing
      • Ju Y.J.
      • Muneta T.
      • Yoshimura H.
      • Koga H.
      • Sekiya I.
      Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing.
      . We have tried to create hematoma over the footprint site at the end of surgery, in expectation of applying the aforementioned effects of hematoma, including platelet-related factors, to promote faster tendon-bone healing and to achieve more stable structural outcomes. In these patients, we often observed that tendon-like tissues formed over the lateral area beyond the footprint where the hematoma was created during the clinical course (Fig. 1). This tendon-healing process leads to a wider footprint and thicker cuff tendon. Confirming the relationship between the presence of hematoma and cuff integrity may indicate the usefulness of hematoma in tendon-bone healing. Before future discussions of tendon quality at the healing site, a first step is to evaluate cuff integrity as a structural outcome on magnetic resonance imaging(MRI) after ARCR.
      Figure thumbnail gr1
      Figure 1The case of a 69-year-old woman who underwent arthroscopic rotator cuff repair (ARCR). a) Intraoperative subacromial view from the lateral portal after suture tying. The lateral part of the decortication area (white arrowhead, red area of c) was exposed. b) The generation of hematoma-like tissue (HLT) is confirmed in the subacromial view. c) Schema for ARCR with the surface-holding method. The decortication area is colored red. d) Schema for generation of HLT after suture tying. HLT is illustrated as the red hatched area. e) Coronal T2-weighted imaging in the slice demonstrating the center of the superior facet at 6 weeks postoperatively. HLT is shown within the red dotted line. f) At 10 months postoperatively, tendon-like tissue has replaced HLT.
      The purposes of this study were thus to investigate the presence and the thickness of hematoma-like tissue (HLT) over the footprint site of ARCR on postoperative MRI and to evaluate the relationship between HLT and structural outcomes for the repaired rotator cuff.

      Materials & Methods

      A prospective cohort study was designed to evaluate the relationship between structural outcomes of the repaired rotator cuff and HLT at the footprint after ARCR. Patients included in this study underwent ARCR surgery for supraspinatus(SSP) tear that size was from small to large with a transosseous method (i.e., the SH method
      • Funakoshi T.
      • Suenaga N.
      • Sano H.
      • Oizumi N.
      • Minami A.
      In Vitro and Finite Element Analysis of a Novel Rotator Cuff Fixation Technique.
      ,
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Araki N.
      • Chosa E.
      Surface-Holding Repair: An Original Arthroscopic Rotator Cuff Repair Technique.
      as described below) in one private hospital between December 2020 and April 2022, in which the formation of HLT was confirmed intraoperatively (Fig. 1), and agreed to participate in the study (i.e., routine MRI follow-up at 1 week, 6–8 weeks, and >6 months postoperatively). The present study was approved by the institutional review board at Hokushin Orthopaedic Hospital (study no. 1905). All surgeries were performed by the same surgeon (co-author, N. S.).

      Surgical technique

      The SH technique is a modified transosseous-equivalent procedure using medial anchors and lateral transosseous sutures, as reported previously
      • Funakoshi T.
      • Suenaga N.
      • Sano H.
      • Oizumi N.
      • Minami A.
      In Vitro and Finite Element Analysis of a Novel Rotator Cuff Fixation Technique.
      ,
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Araki N.
      • Chosa E.
      Surface-Holding Repair: An Original Arthroscopic Rotator Cuff Repair Technique.
      . All patients underwent preoperative interscalene block under general anesthesia. All procedures were performed in the beach chair position. During the surgical procedure, bursectomy was performed and other intervening tissues (residual remnant of the tendon or scar tissue) were perfectly removed from the footprint site. Anterior acromioplasty was performed with excision of the coracoacromial ligament as described by Ellman
      • Ellman H.
      Arthroscopic Subacromial Decompression: Analysis of One- to Three-Year Results.
      . The new footprint was created from 5-7 millimeters medial to the original footprint by removing cartilage and cortical and subchondral bone until the cancellous bone was completely exposed. Bone marrow stimulation(BMS) was also performed at the footprint; that is, the area between the suture anchors and pull-out tunnels
      • Ajrawat P.
      • Dwyer T.
      • Almasri M.
      • Veillette C.
      • Romeo A.
      • Leroux T.
      • et al.
      Bone marrow stimulation decreases retear rates after primary arthroscopic rotator cuff repair: a systematic review and meta-analysis.
      ,
      • Bilsel K.
      • Yildiz F.
      • Kapicioglu M.
      • Uzer G.
      • Elmadag M.
      • Pulatkan A.
      • et al.
      Efficacy of bone marrow-stimulating technique in rotator cuff repair.
      ,
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Yamaguchi H.
      • Inoue K.
      • et al.
      Bone marrow stimulation at the footprint of arthroscopic surface-holding repair advances cuff repair integrity.
      . The extent of medialization was defined depending on the tension of the repaired tendon. Following adequate mobilization of the torn tendon, the tendon was repaired at the footprint under no excessive tension with the arm positioned at the side (Fig. 1a). During suture tying after pull-out of the anchor threads at the lateral side of greater tuberosity, intraarticular perfusion was stopped to induce HLT formation. After suture tying, HLT formation was confirmed in a subacromial view with low perfusion pressure (Fig. 1b).

      Postoperative treatment

      Postoperatively, an abduction brace was used for 6 or 8 weeks according to the condition, tear size, quality, and tension of the repaired tendon. Further, a systematic postoperative rehabilitation program was conducted with self-assisted ROM exercises 1 day or 2 weeks postoperatively. Anti-gravity active elevation was permitted after 8–10 weeks, while isometric cuff exercises were initiated at 10–12 weeks. Patients were allowed to fully return to heavy work or sports after passing an assessment to confirm sufficient recovery of muscle strength and range of motion at 6 months postoperatively.

      Patients and evaluation

      Twenty-eight patients agreed to be registered to the study. One patient who experienced severe complications unrelated to the shoulder surgery was excluded. Two patients who demonstrated rotator cuff retear (i.e., Sugaya classification
      • Sugaya S.
      • Maeda K.
      • Matsuki K.
      • Moriishi J.
      Repair integrity and functional outcome after arthroscopic double-row rotator cuff repair. A prospective outcome study.
      types 4 and 5) at 1 and 6 weeks postoperatively were also excluded. As a result, 25 patients (18 men, 7 women) were able to be reviewed. Mean age of patients at the time of surgery was 69.8 years (range, 52–85 years). Tear size was classified intraoperatively using the system described by DeOrio and Cofield, as follows: small, <1 cm; medium, 1–3 cm; large, 3–5 cm; and massive, >5 cm or involving two tendons
      • DeOrio J.K.
      • Cofield R.H.
      Results of a second attempt at surgical repair of a failed initial rotator-cuff repair.
      ,
      • Galatz L.M.
      • Ball C.M.
      • Teefey S.A.
      • Middleton W.D.
      • Yamaguchi K.
      The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears.
      . Preoperative atrophy of torn cuff muscle according to Yamaguchi's classification
      • Yamaguchi H.
      • Suenaga N.
      • Oizumi N.
      • Hosokawa Y.
      • Kanaya F.
      Will preoperative atrophy and Fatty degeneration of the shoulder muscles improve after rotator cuff repair in patients with massive rotator cuff tears?.
      andfatty degeneration of cuff muscle according to Goutallier's classification were also evaluated on preoperative MRI images.
      Postoperative MRI was performed in all patients at 1 week, 6–8 weeks (at the time of brace removal), and >6 months postoperatively using a 1.5-T closed-type scanner (EXCELART Vantage powered by Atlas or VISART/EX; Toshiba, Ohtawara, Japan). Coronal T2-weighted images were acquired for structural assessment of the rotator cuff tendons and HLT, as described in previous reports that discussed structural outcomes after ARCR
      • Malavolta E.A.
      • Assunção J.H.
      • Ramos F.F.
      • Ferreira T.C.
      • Gracitelli M.E.C.
      • Rodrigues M.B.
      • et al.
      Serial structural MRI evaluation of arthroscopy rotator cuff repair: does Sugaya's classification correlate with the postoperative clinical outcomes?.
      ,
      • Muniandy M.
      • Niglis L.
      • Dosch J.C.
      • Meyer N.
      • Kempf J.F.
      • Collin P.
      • et al.
      Postoperative rotator cuff integrity: can we consider type 3 Sugaya classification as retear?.
      ,
      • Sugaya S.
      • Maeda K.
      • Matsuki K.
      • Moriishi J.
      Repair integrity and functional outcome after arthroscopic double-row rotator cuff repair. A prospective outcome study.
      ,
      • Yoshida M.
      • Collin P.
      • Josseaume T.
      • Lädermann A.
      • Goto H.
      • Sugimoto K.
      • et al.
      Post-operative rotator cuff integrity, based on Sugaya's classification, can reflect abduction muscle strength of the shoulder.
      . Coronal T2-weighted fat-suppressed images were also acquired to evaluate signal intensity of the SSP and HLT, referring to a previous report
      • Ishitani E.
      • Harada N.
      • Sonoda Y.
      • Okada F.
      • Yara T.
      • Katsuki I.
      Tendon stump type on magnetic resonance imaging is a predictive factor for retear after arthroscopic rotator cuff repair.
      . Signal intensity was measured using the measuring tool in EV insite (PSP, Tokyo, Japan). Structural outcomes for the repaired cuff were evaluated with Sugaya’s classification on coronal T2-weighted images at >6 months postoperatively. Thickness of the HLT was evaluated on coronal T2-weighted images in the slice demonstrating the center of the superior facet, and was classified into three grades as follows: Grade 1, absence of the HLT (Fig. 2a); Grade 2, HLT thickness not exceeding the line connecting the surface of the rotator cuff and the lateral edge of the greater tuberosity (Fig. 2b); and Grade 3; HLT thickness exceeding the line connecting the surface of the rotator cuff and the lateral edge of the greater tuberosity (Fig. 2c). Thickness grade of the HLT was evaluated at 1 and 6 weeks postoperatively. Signal intensities of the SSP and HLT were evaluated on coronal T2-weighted fat-suppressed image sequences at the slice demonstrating the center of the superior facet (Fig. 3). Intensity of the SSP was evaluated at a point 1 cm medial to the tendon end. Intensity of the HLT was evaluated at the lateral end of the HLT (Fig. 3). Signal intensities were measured as the mean value for a circle with a diameter of 5 mm2 at these points. Intensity was measured twice at each point, and the average of the two measurements was calculated. The ratio of HLT intensity to SSP intensity (HLT/SSP ratio) was calculated at each MRI.
      Figure thumbnail gr2
      Figure 2Grading of the thickness of hematoma-like tissue (HLT) (blue dotted line). a) Grade 1, absence of the HLT. b) Grade 2, thickness of HLT does not exceed the line connecting the surface of the rotator cuff and the lateral edge of the greater tuberosity. c) Grade 3, thickness of HLT exceeds the line connecting the surface of the rotator cuff and the lateral edge of the greater tuberosity.
      Figure thumbnail gr3
      Figure 3Signal intensity as evaluated on coronal T2-weighted fat-suppressed imaging. Intensity of the SSP is evaluated at a point 1 cm medial to the end of the tendon (red arrow). The intensity of HLT (blue dotted line) is evaluated at a point at the lateral end of the HLT (blue arrow).

      Analysis

      Univariate analyses of HLT thickness were performed among Sugaya classification types (type I vs. II vs. III). Preoperative factors were also analyzed among Sugaya types, that included age, sex, smoking habit defined in Maloon’s report
      • Mallon W.J.
      • Misamore G.
      • Snead D.S.
      • Denton P.
      The impact of preoperative smoking habits on the results of rotator cuff repair.
      , the size of tear, atrophy and fatty degeneration of torn cuff. HLT/SSP ratios were compared among the timings of postoperative MRI (1 week vs. 6–8 weeks vs. >6 months), among Sugaya classification types (type I vs. II vs. III), and between thickness grades (grade 2 vs. 3).

      Statistical analyses

      The Mann-Whitney U test was used to evaluate quantitative data, and Fisher's exact probability test was used for categorical data. Signal intensity was compared using the Wilcoxon signed-rank test. Values of p <.05 were considered significant for both uni- and multivariate analyses. Multigroup comparisons and Bonferroni correction were used to compare results between three groups. All statistical analyses were performed using R software (The R Foundation for Statistical Computing, Vienna, Austria).

      Results

      At >6 months postoperatively, structural evaluation of the repaired cuff by the Sugaya classification showed type 1 in 12 shoulders, type 2 in 4, and type 3 in 9. Thickness grade of the HLT at 1 week postoperatively was grade 1 in 7 shoulders, grade 2 in 7, and grade 3 in 11. Grade at 6–8 weeks postoperatively was grade 1 in 8 shoulders, grade 2 in 11, and grade 3 in 6. Table I shows changes over time in thickness of the HLT from 1 week postoperatively to 6–8 weeks postoperatively. HLT became thinner in 4 shoulders and disappeared in 3 shoulders from 1 week to 6–8 weeks. In contrast, HLT formed in 2 shoulders from 1 week to 6–8 weeks. HLT did not become thicker (from grade 2 to grade 3) from 1 week to 6–8 weeks in any cases. HLT thickness at 1 week and 6–8 weeks postoperatively was significantly larger in patients with Sugaya type 1 than in those with type 3 (1 week ; p=.014, 6-8 weeks ; p<.001) (Table II). Age, sex, rotator cuff tear size, atrophy and fatty degeneration of torn cuff and HLT thickness at 1 week postoperatively showed no significant differences. Postoperatively, mean signal intensity of the HLT decreased gradually and became closer to that of SSP (HLT/SSP ratio at 1 week postoperatively: 1.9±0.7; at 6–8 weeks postoperatively: 1.6±0.6; at >6 months postoperatively: 1.2±0.5). HLT/SSP ratio differed significantly between 1 week and >6 months postoperatively (p<.001), and between 6–8 weeks and >6 months postoperatively (p<.001) (Fig. 4). HLT/SSP ratio did not differ significantly between Sugaya classification types (type I: 1.1±0.5; type II: 1.3±0.4; type III: 1.2±0.6) or thickness grades (grade 2: 1.9±0.7; grade 3: 1.7±0.6; p=.43).
      Table ITemporal changes in thickness of hematoma-like tissue
      Table thumbnail fx1
      Data are expressed as the number of shoulders.
      Table IIUnivariate analyses within each subtype of Sugaya’s classification
      VariableSugayaI (n=12)SugayaII (n=4)SugayaIII (n=9)P value
      I vs IIII vs IIII vs III
      Age (years)70.1±8.169.5±13.670.3±5.2.90>.99.94
      Sex (male/female)10/23/15/4>.99>.99.33
      smoking3(25.0%)1(25.0%)2(22.2%)>.99>.99>.99
      Rotator cuff tear size
       small01(25.0%)0.15.64.64
       medium8(66.6%)3(75.0%)4(44.4%)
       large4(33.3%)05(55.6%)
      Yamaguchi’s classification(%)2.3±0.72.5±0.62.7±0.5.68.58.23
      Goutallier’s classification1.75±0.91.25±0.51.78±0.7.31.17.82
      HLT thickness at 1week postoperatively
       Grade11(8.3%)2(50.0%)4(44.4%).12>.99.014*
       Grade22(16.7%)1(25.0%)4(44.4%)
       Grade39(75.0%)1(25.0%)1(11.1%)
      HLT thickness at 6weeks postoperatively
       Grade102(50.0%)9(100.0%).032.077<.001*
       Grade26(50.0%)2(50.0%)0
       Grade36(50.0%)00
      Data are expressed as the number of shoulders or as mean±standard deviation.
      *P < .0167 after Bonferroni correction.
      Figure thumbnail gr4
      Figure 4Box-and-whisker plot of the ratio of hematoma-like tissue (HLT) intensity on magnetic resonance imaging to that of the supraspinatus (SSP) tendon. Top and bottom borders of boxes represent the interquartile range, with the center line representing the median. Whiskers represent the minimum and maximum values. Intensity of the HLT gradually decreases and becomes closer to that of the SSP tendon. Intensity is significantly different between 1 week and >6 months (*p<.001), and between 6–8 weeks and >6 months (*p<.001). HLT, hematoma-like tissue; SSP, supraspinatus.

      Discussion

      In the present study, the presence of HLT and the relationship between the HLT and the structural outcome of the repaired rotator cuff tendon was investigated as the first step toward proving the usefulness of HLT in tendon-bone healing. As a result, cases with thicker HLT at 6 weeks after surgery displayed better structural outcomes at >6 months after surgery.
      To improve retear rates and structural outcomes, various suturing methods have been devised based on biomechanical considerations, and BMS has been added to those procedures in consideration of biological factors
      • Taniguchi N.
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      • Miyoshi N.
      • Yamaguchi H.
      • Inoue K.
      • et al.
      Bone marrow stimulation at the footprint of arthroscopic surface-holding repair advances cuff repair integrity.
      .
      Fibrin clots have been used to enhance the healing of various musculoskeletal tissues, including meniscus, cartilage, and ligaments
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      . These clots are made using blood from the patient, so the costs are reasonable. Fibrin clots are expected to provide necessary properties for both structural support and delivery of platelet-derived growth factors
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      ,
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      (2013) Arthroscopic inside-out repair of complete radial tears of the meniscus with a fibrin clot.
      . In the knee, anterior cruciate ligament reconstruction adding a fibrin clot to the allograft reduces the amount of tunnel widening seen at the 1-year follow-up
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      . Fibrin clot is also reported to promote meniscus fusion
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      • Maffulli N.
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      • Ra H.J.
      • Ha J.K.
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      • Kim J.G.
      (2013) Arthroscopic inside-out repair of complete radial tears of the meniscus with a fibrin clot.
      and healing rate
      • Ra H.J.
      • Ha J.K.
      • Jang S.H.
      • Lee D.W.
      • Kim J.G.
      (2013) Arthroscopic inside-out repair of complete radial tears of the meniscus with a fibrin clot.
      . In the shoulder, platelet-containing plasma derivatives, most notably platelet-rich plasma (PRP), are among the options for biological augmentation of rotator cuff repair. Platelets isolated in the plasma layer have been shown to release a host of cytokines and growth factors that can aid in tendon healing
      • Andia I.
      • Sanchez M.
      • Maffulli N.
      Platelet rich plasma therapies for sports muscle injuries: Any evidence behind clinical practice?.
      . Kobayashi reported that platelet-derived growth factor increased the early tensile strength of rotator cuff repairs in sheep models
      • Kobayashi M.
      • Itoi E.
      • Minagawa H.
      • Miyakoshi N.
      • Takahashi S.
      • Tuoheti Y.
      • et al.
      Expression of growth factors in the early phase of supraspinatus tendon healing in rabbits.
      . Use of the platelet-leukocyte membrane in the treatment of rotator cuff tears improved repair integrity when compared with repair without the membrane
      • Gumina S.
      • Campagna V.
      • Ferrazza G.
      • Giannicola G.
      • Fratalocchi F.
      • Milani A.
      • et al.
      Use of plateletleukocyte membrane in arthroscopic repair of large rotator cuff tears: A prospective randomized study.
      . Based on these reports, we attempted to introduce hematoma in ARCR methods to promote tendon-bone healing by creating HLT at the lateral site of the footprint.
      In the history of suture methods for ARCR, a single-row method was reported in the 1990s
      • Snyder S.J.
      Technique of arthroscopic rotator cuff repair using implantable 4-mm Revo suture anchors, suture Shuttle Relays, and no. 2 nonabsorbable mattress sutures.
      ,
      • Thal R.
      A technique for arthroscopic mattress suture placement.
      as a suture method using a medial anchor first. To achieve stronger fixation of the tendon ends and a larger contact area of the sutured rotator cuff, the double-row technique was reported by Lo and Burkhart in 2003
      • Lo IKY Ian K.Y.
      • Burkhart S.S.
      Double-row arthroscopic rotator cuff repair: re-establishing the footprint of the rotator cuff.
      . Transosseous-equivalent methods as represented by the suture bridge technique
      • Park M.C.
      • Elattrache N.S.
      • Ahmad C.S.
      • Tibone J.E.
      Transosseous-equivalent" rotator cuff repair technique.
      have since been developed to achieve minimal invasiveness in arthroscopic surgery while offering results similar to open surgery in terms of anatomical physiology and biomechanics
      • Kuroda S.
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      • Mikasa M.
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      ,
      • Park M.C.
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      • Waltrip R.L.
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      . However, in the suture bridge technique, the strong compression force may cause overstraining and ischemia of the rotator cuff, and, in cases with insufficient reduction of the cuff, the compression force tends to be inadequate. Considering the advantages of inducing fibrin clot in ARCR, Funakoshi and Suenaga et al reported the SH method
      • Funakoshi T.
      • Suenaga N.
      • Sano H.
      • Oizumi N.
      • Minami A.
      In Vitro and Finite Element Analysis of a Novel Rotator Cuff Fixation Technique.
      ,
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Araki N.
      • Chosa E.
      Surface-Holding Repair: An Original Arthroscopic Rotator Cuff Repair Technique.
      ,
      • Yamaguchi H.
      • Suenaga N.
      • Oizumi N.
      • Hosokawa Y.
      • Kanaya F.
      Open repair for massive rotator cuff tear with a modified transosseousequivalent procedure: preliminary results at short-term follow-up.
      as a modified transosseous-equivalent procedure using medial anchors and lateral transosseous sutures to improve the biomechanical properties of rotator cuff repair. In this method, the new footprint was created 5-7 millimeters medial to the original footprint to reduce excessive suture tension to the tendon in all cases, and decortication was performed at the new and original footprint and beyond lateral to the edge of the greater tuberosity. In addition, Taniguchi et al reported that the retear rate was reduced by adding BMS to this procedure
      • Taniguchi N.
      • Suenaga N.
      • Oizumi N.
      • Miyoshi N.
      • Yamaguchi H.
      • Inoue K.
      • et al.
      Bone marrow stimulation at the footprint of arthroscopic surface-holding repair advances cuff repair integrity.
      . These procedures were expected to induce mesenchymal stem cells that allow potential for differentiation into tendon tissues
      • Caplan A.I.
      Why are MSCs therapeutic? New data: new insight.
      and accelerate early remodeling during tendon-bone healing
      • Ju Y.J.
      • Muneta T.
      • Yoshimura H.
      • Koga H.
      • Sekiya I.
      Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing.
      . Further, an ultrasound study revealed blood flow from the footprint during 3 months after the SH method
      • Funakoshi T.
      • Iwasaki N.
      • Kamishima T.
      • Nishida M.
      • Ito Y.
      • Nishida K.
      • et al.
      In vivo vascularity alterations in repaired rotator cuffs determined by contrast-enhanced ultrasound.
      . Based on such findings, HLT formation seems to have potential for providing advantageous tendon repair.
      With improvements in MRI performance, more detailed evaluations of the rotator cuff have become available to determine signal intensity
      • Ishitani E.
      • Harada N.
      • Sonoda Y.
      • Okada F.
      • Yara T.
      • Katsuki I.
      Tendon stump type on magnetic resonance imaging is a predictive factor for retear after arthroscopic rotator cuff repair.
      ,
      • Lo H.C.
      • Hung S.T.
      • Kuo D.P.
      • Chen Y.L.
      • Lee H.M.
      Quantitative diffusion-weighted magnetic resonance imaging for the diagnosis of partial-thickness rotator cuff tears.
      ,
      • Xie Y.
      • Liu S.
      • Qu J.
      • Wu P.
      • Tao H.
      • Chen S.
      Quantitative Magnetic Resonance Imaging UTE-T2* Mapping of Tendon Healing After Arthroscopic Rotator Cuff Repair: A Longitudinal Study.
      and structural outcomes after ARCR
      • Galatz L.M.
      • Ball C.M.
      • Teefey S.A.
      • Middleton W.D.
      • Yamaguchi K.
      The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears.
      ,
      • Jost B.
      • Zumstein M.
      • Pfirrmann C.W.
      • Gerber C.
      Long-term outcome after structural failure of rotator cuff repairs.
      ,
      • Sugaya S.
      • Maeda K.
      • Matsuki K.
      • Moriishi J.
      Repair integrity and functional outcome after arthroscopic double-row rotator cuff repair. A prospective outcome study.
      . Moreover, the progression of tendon healing can be surveilled dynamically using longitudinal studies with MRI
      • Iannotti J.P.
      • Deutsch A.
      • Green A.
      • Rudicel S.
      • Christensen J.
      • Marraffino S.
      • et al.
      Time to failure after rotator cuff repair: a prospective imaging study.
      ,
      • Koh K.H.
      • Laddha M.S.
      • Lim T.K.
      • Park J.H.
      • Yoo J.C.
      Serial structural and functional assessments of rotator cuff repairs: do they differ at 6 and 19 months postoperatively?.
      . In the comparison among Sugaya types 1–3, higher Sugaya type was found to be associated with longer duration of symptoms
      • Paul S.
      • Goyal T.
      • Yadav A.K.
      Association between functional outcome scores and MRI-based structural integrity after rotator cuff repair: a prospective cohort study.
      . Considering these reports, the presence of HLT and relationships between HLT and structural outcomes for the repaired tendon were also discussed based on MRI in the present study.
      Thickness of the HLT became thinner in 28.0% of all shoulders from 1 week to 6-8 weeks. In the SH method, as mentioned before, blood flow continues from the footprint during 3 months after the operation
      • Funakoshi T.
      • Iwasaki N.
      • Kamishima T.
      • Nishida M.
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      • Nishida K.
      • et al.
      In vivo vascularity alterations in repaired rotator cuffs determined by contrast-enhanced ultrasound.
      , predicting the possibility of an increased grade of HLT thickness, however, a result of HLT thinning may suggest compositional changes to the hematoma. Signal intensity of the HLT gradually decreased to become closer to that of the SSP. Changes in hematoma signal also suggest compositional changes in HLT, such as loss of the fluid element and increased organization. HLT thickness at 1 week and 6–8 weeks postoperatively was significantly larger in Sugaya type 1 patients than in type 3 patients. In those cases, a wide footprint area, extending laterally from the footprint made during surgery, was seen on MRI at >6 months, and the repaired tendon was sufficiently thick as a result. Regarding the relationship between clinical and structural outcomes of the repaired cuff tendon, some reports have demonstrated a correlation between Sugaya classification
      • Sugaya S.
      • Maeda K.
      • Matsuki K.
      • Moriishi J.
      Repair integrity and functional outcome after arthroscopic double-row rotator cuff repair. A prospective outcome study.
      and clinical outcomes of muscle strength score
      • Yoshida M.
      • Collin P.
      • Josseaume T.
      • Lädermann A.
      • Goto H.
      • Sugimoto K.
      • et al.
      Post-operative rotator cuff integrity, based on Sugaya's classification, can reflect abduction muscle strength of the shoulder.
      , and pain
      • Malavolta E.A.
      • Assunção J.H.
      • Ramos F.F.
      • Ferreira T.C.
      • Gracitelli M.E.C.
      • Rodrigues M.B.
      • et al.
      Serial structural MRI evaluation of arthroscopy rotator cuff repair: does Sugaya's classification correlate with the postoperative clinical outcomes?.
      . Bonnevialle et al reported significantly lower microvascularization of the footprint in the retear group than in the healing group with an immunohistochemical technique using anti-CD34 antibodies. This report also suggested that bone microvascularization of the footprint plays a role in rotator cuff healing, and affects tendon integrity after repair
      • Bonnevialle N.
      • Bayle X.
      • Faruch M.
      • Wargny M.
      • Brouchet A.G.
      • Mansat P.
      Does microvascularization of the footprint play a role in rotator cuff healing of the shoulder?.
      . If HLT thickness in this study reflected microvascularization of the footprint, the result that Sugaya type 1 patients showed a larger HLT corresponds to the report by Bonnevialle
      • Bonnevialle N.
      • Bayle X.
      • Faruch M.
      • Wargny M.
      • Brouchet A.G.
      • Mansat P.
      Does microvascularization of the footprint play a role in rotator cuff healing of the shoulder?.
      . In this case series, one case demonstrated Sugaya type 1 despite grade 1 thickness of the HLT at 1 week postoperatively. This may indicate that other factors are related to improving cuff integrity after ARCR.
      The term “crimson duvet” was first used by Snyder in 2009
      • Snyder S.J.
      • Burns J.
      Rotator cuff healing and the bone marrow ‘‘crimson duvet’’ from clinical observation to science.
      to describe a reddish-purple clot that issues from small “bone marrow vents” punctured in the cortex of the greater tuberosity during rotator cuff repair
      • Galatz L.M.
      • Ball C.M.
      • Teefey S.A.
      • Middleton W.D.
      • Yamaguchi K.
      The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears.
      ,
      • Jost B.
      • Zumstein M.
      • Pfirrmann C.W.
      • Gerber C.
      Long-term outcome after structural failure of rotator cuff repairs.
      ,
      • Wong I.
      • Burns J.
      • Snyder S.
      Arthroscopic GraftJacket repair of rotator cuff tears.
      , enveloping the repair site and acting to regenerate the footprint of the rotator cuff
      • Milano G.
      • Saccomanno M.F.
      • Careri S.
      • Taccardo G.
      • De Vitis R.
      • Fabbriciani C.
      Efficacy of marrow-stimulating technique in arthroscopicrotator cuff repair: a prospective randomized study.
      . This blanket of super-clot can provide cells, growth factors, and matrix in an efficient manner. In a mouse chimeric model, bone marrow-derived cells infiltrated the repaired rotator cuff and contributed to postoperative rotator cuff healing
      • Kida Y.
      • Morihara T.
      • Matsuda K.-I.
      • Kajikawa Y.
      • Tachiiri H.
      • Iwata Y.
      • et al.
      Bone marrow derived cells from the footprint infiltrate into the repaired rotator cuff.
      . The relationship between the term “crimson duvet” and HLT in this study remains uncertain, however, a histological study of HLT may reveal the real identity of HLT. HLT seemed to substitute to tendon on MRI in many cases, however, the actual phenomenon involved and the mechanism contributing in these cases was not clarified in the present study. The obvious fact demonstrated in this report was the statistical relationship between thickness of the HLT and structural outcomes after ARCR. In other words, obtaining a thicker HLT after surgery offers an expectation of good structural outcomes with Sugaya type 1 integrity of the repaired cuff tendon, which relates to good clinical outcomes. If so, to achieve better structural outcome, methods to gain a thicker HLT must be discussed, such as the use of certain epidermal factors (i.e., PRP), a certain period of non-mobilization after surgery, or expansion of the BMS area more laterally.

      Limitations

      Some limitations to this study need to be considered. First, this study is a preliminary research including only a small number of cases. Evaluation of a larger number of cases in each group would provide stronger statistical support, although some results were statistically significant in this study. Second, as already mentioned, the histological behavior of HLT is unclear despite our hypothesis that HLT represents the same tissue as hematoma on the footprint observed during surgery. Lastly, this study was based solely on structural outcomes apparent on MRI, and did not evaluate mechanical strength of the resulting tendon.

      Conclusions

      In the present study, the presence of HLT and the relationship between the HLT and structural outcomes of the repaired rotator cuff were confirmed. HLT on outside the footprint with the arthroscopic SH method showed a signal intensity becoming more similar to that of the SSP tendon over time. Cases with thicker HLT at 1 week and 6-8 weeks after surgery can be expected to show good structural outcomes at >6 months after surgery.

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