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Comparison of a Novel Bone-Tendon Allograft With a HumanDermis–Derived Patch for Repair of Chronic Large Rotator Cuff
Tears Using a Canine Model
Matthew J. Smith, M.D., James L. Cook, D.V.M., Ph.D., Keiichi Kuroki, D.V.M., Ph.D.,Prakash S. Jayabalan, M.D., Cristi R. Cook, D.V.M., M.S., Ferris M. Pfeiffer, Ph.D., and
Nicole P. Waters, M.S.
Purpose: This study tested a bone-tendon allograft versus human dermis patch for reconstructing chronicrotator cuff repair by use of a canine model. Methods: Mature research dogs (N � 15) were used.Radiopaque wire was placed in the infraspinatus tendon (IST) before its transection. Three weeks later,radiographs showed IST retraction. Each dog then underwent 1 IST treatment: debridement (D), directrepair of IST to bone with a suture bridge and human dermis patch augmentation (GJ), or bone-tendonallograft (BT) reconstruction. Outcome measures included lameness grading, radiographs, and ultrasono-graphic assessment. Dogs were killed 6 months after surgery and both shoulders assessed biomechanicallyand histologically. Results: BT dogs were significantly (P � .01) less lame than the other groups. BT dogshad superior bone-tendon, tendon, and tendon-muscle integrity compared with D and GJ dogs. Biome-chanical testing showed that the D group had significantly (P � .05) more elongation than the other groupswhereas BT had stiffness and elongation characteristics that most closely matched normal controls.Radiographically, D and GJ dogs showed significantly more retraction than BT dogs (P � .003 and P �.045, respectively) Histologically, GJ dogs had lymphoplasmacytic infiltrates, tendon degeneration andhypocellularity, and poor tendon-bone integration. BT dogs showed complete incorporation of allograftbone into host bone, normal bone-tendon junctions, and well-integrated allograft tendon. Conclusions:The bone-tendon allograft technique re-establishes a functional IST bone-tendon-muscle unit and main-tains integrity of repair in this model. Clinical Relevance: Clinical trials using this bone-tendon allografttechnique are warranted.
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Rotator cuff injuries requiring treatment are a com-mon clinical problem. Massive rotator cuff tears
ay account for approximately 30% of surgicallyepaired rotator cuff tears.1 Treatments for large to
From the Department of Orthopaedic Surgery (M.J.S.) and Com-parative Orthopaedic Laboratory (J.L.C., K.K., P.S.J., C.R.C., F.M.P.,N.P.W.), University of Missouri, Columbia, Missouri, U.S.A.
Supported by Community Tissue Services, Dayton, OH. Theauthors report no conflict of interest.
Received January 7, 2011; accepted August 16, 2011.Address correspondence to Matthew J. Smith, M.D., Department
of Orthopaedic Surgery, University of Missouri, 1100 VirginiaAve, DC953.00, Columbia, MO 65212, U.S.A. E-mail: [email protected]
© 2012 by the Arthroscopy Association of North America
a0749-8063/1118/$36.00doi:10.1016/j.arthro.2011.08.296
Arthroscopy: The Journal of Arthroscopic and Related Su
massive chronic rotator cuff tears have not yieldedconsistently good results, with failure rates as high as94% reported in some studies.2 Many factors are asso-iated with poor outcomes, including tendon retraction,uscle atrophy and fatty degeneration, and poor tissue
uality, causing disruption and dysfunction of the muscle-endon-bone unit.3 As such, documented tendon-to-
bone healing and long-term functional success ratesfor these types of tears are low.4
Authors have described direct tendon-to-bone su-ture repair techniques of various types,5-10 tendonransfers, and soft-tissue augmentation techniques.urrently, the most commonly used surgical treatment
s direct repair of native tendon to bone wheneverossible. However, for massive tears, direct repair is
ssociated with biomechanically inferior repair con-169rgery, Vol 28, No 2 (February), 2012: pp 169-177
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170 M. J. SMITH ET AL.
structs, exhibiting only 18% and 31% of the strengthof the normal rotator cuff at 6 and 12 weeks afterrepair, respectively.11 Failure to re-establish a normalbone-tendon junction appears to be a primary reasonfor the inability to regain functional rotator cuff repairand the resultant failures.12,13 When such tears are notepairable or completely repairable, a number of sur-ical options are currently used for pain relief, includ-ng subacromial decompression, tuberoplasty, bicepsenotomy, or debridement alone.14,15
As such, various biomaterials have been developed,tested, and used clinically in an attempt to augmentthe surgical repair, speed healing, mitigate failures,and improve functional outcomes.16 Recently, someuthors have reported success with “rotator cuff re-lacement” by spanning tendon defects using dermalllograft.4 In a small series of cases, anecdotal out-omes of this technique were reported to be good toxcellent in 75% of patients. However, current bio-aterials used to augment surgical rotator cuff repairs
re not intended or approved for use as “span” orstructural” grafts, because they are heterotopic allo-rafts or xenografts that have inferior biomechanicalroperties, have poor incorporation characteristics,nd/or engender untoward immune or inflammatoryesponses.16-22 Recapitulation of normal tendon-bone
attachment and function is not attained by use ofcurrent techniques and likely will only be accom-plished by addressing structure, function, and healingas comprehensively as is possible.
In a previous study, we reported promising resultsfor rotator cuff repair in a canine infraspinatus tendon(IST) model using a bone-tendon allograft implant andtechnique.23 The bone-tendon allograft technique wasassociated with highly functional healing of the in-fraspinatus muscle-tendon-bone unit in an acute resec-tion model based on clinical, imaging, biomechanical,and histologic outcome measures. However, in theclinical setting the quality of the remaining tendonsand musculature is often poor because of degenera-tion, fatty infiltration, and retraction.24-26 Thereforehe objective of this study was to test our bone-tendonllograft technique for reconstructing chronic largeotator cuff defects using a canine model and comparehe results with 2 current standard-of-care treatments,hen simple repair is no longer possible—(1) direct
epair and augmentation with a commercially avail-ble human dermis patch (GraftJacket; Wright Medi-al Technology, Arlington, TN) and (2) debridementlone—using functional, imaging, histologic, and bio-echanical outcome measures. The hypothesis was
hat because of its bone-to-bone fixation, the bone-
endon allograft would provide superior biomechani-al and clinical results compared with the other repairroups.
METHODS
All procedures were approved by our university’snimal care and use committee.
The proximal humerus with the supraspinatus, in-raspinatus, and teres minor muscle-tendon units at-ached were harvested from adult canine cadavers (Fig). The tissues were wrapped in sterile saline solu-ion–soaked gauze sponges, double wrapped in sterileags, and shipped by overnight courier to Communityissue Services (Dayton, OH), where they were pro-essed for implantation by current standard-of-careroprietary procedures for human tendon-bone allo-rafts. The grafts were then packaged in sterile double-rapped sealed surgical packaging and returned to the
aboratory by overnight courier.Mature purpose-bred dogs (N � 15) were used for
n vivo study. The dogs were premedicated, anesthe-ized, and prepared for aseptic surgery of the righthoulder. Through a 2-cm incision over the proximalumerus, the right IST of each dog was identified andsolated. A radiopaque marker wire was placed ap-roximately 5 mm caudal to its insertion, and then theendon was completely transected at its insertion andllowed to retract. Radiographs were obtained afteretraction to document the degree of tendon retraction,nd measurements of IST insertion-to-marker distanceere made on calibrated images.Three weeks after tendon transection, the dogs were
gain premedicated, anesthetized, and prepared forseptic surgery of the right shoulder. Radiographs of
FIGURE 1. Canine rotator cuff tissue harvests for grafts. (IS,
infraspinatus; SS, supraspinatus; TM, teres minor.)
so
171BONE-TENDON ALLOGRAFT FOR ROTATOR CUFF TEARS
the right shoulders were again obtained, and each dogunderwent surgical treatment of the right IST. The ISTwas treated by debridement of proliferative fibroustissue (n � 5) (D), direct repair of the tendon to bonewith a suture-bridge technique and a human dermispatch augmentation (GraftJacket) (n � 5) (GJ), or thebone-tendon allograft technique (n � 5) (BT). In theGraftJacket group, none of the retracted tendons cov-ered the actual footprint, but they were partially re-
FIGURE 2. (A) Bone trough and retracted torn tendon edge. (B)utures passed through bone-tendon junction of allograft. (D) Finaver bone block.
paired to bone as much as possible. The remaining
footprint was then covered and the tendon augmentedwith GraftJacket to complete a suture-bridge con-struct.
Rotator cuff grafts were aseptically created by sharpdissection and an oscillating saw. The grafts weretreated through a proprietary bioburden reduction pro-cess (Allowash; LifeNet Health, Virginia Beach, VA),frozen at �70°C, terminally sterilized with gammairradiation (delivered dose, 1.7 to 2.1 Mrad), and then
ent of medial anchors along articular margin. (C) Medial anchorr with allograft tendon to native tendon sutures and suture bridge
Placeml repai
stored frozen until the time of surgery. In the allograft
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172 M. J. SMITH ET AL.
the tendon was not repaired back to bone at all. Thetendon edge was mobilized, and the lateral edge ofthe tendon was repaired to the tendinous portion of theallograft. The allograft bone was secured to the bonyfootprint by use of suture anchor fixation in a suture-bridge pattern, compressing the bone into a preparedbed (Fig 2). Postoperative radiographs of the rightshoulders were then obtained (Fig 3), and measure-ments of IST insertion-to-marker distance were madeon calibrated images (Table 1).
After surgery, the dogs were allowed full weightbearing but were restricted to kennel rest for 6 weeksand then allowed enrichment activities.
Temporal outcome measures included lamenessevaluation at 0, 4, 8, 12, and 24 weeks; radiographs at0, 4, 12, and 24 weeks; and ultrasonographic assess-
TABLE 1. IST Insertion-to-Marker Distances Me
Retracted*
D GJ BT D
Mean (cm) 2.59 � 0.24 2.51 � 0.21 2.54 � 0.26 2.60 � 0.2
*No significant difference (P � .85; power, 0.49).†The value in the D group was significantly greater than those
and BT groups showed no significant differences.
‡The value in the D group was significantly greater than those in the Gn the GJ group was significantly greater than that in the BT group (P �
ment at 0, 12, and 24 weeks. Measurements of ISTinsertion-to-marker distance were made on calibratedimages. Magnetic resonance imaging (MRI) was per-formed in 1 dog from each treatment group and 1normal contralateral shoulder for subjective clinicalcorrelation to postoperative imaging in humans.
Dogs were killed by humane euthanasia at 6 monthsafter surgery. Operated and nonoperated shoulderswere assessed biomechanically for stiffness and dis-placement during cyclic mechanical testing and forhistologic appearance.
To apply and directly compare all outcome mea-sures used in this study for all shoulders, nonde-structive biomechanical testing was performed. TheIST bone-tendon-muscle complex was excised enbloc, with attachments to the scapula left intact. The
FIGURE 3. Intraoperative im-ages and postoperative radio-graphs for each treatment group.
on Calibrated Radiographs at Each Time Point
paired† 6 mo‡
GJ BT D GJ BT
6 � 0.16 1.42 � 0.17 3.78 � 0.41 2.56 � 0.73 1.71 � 0.33
J and BT groups (P � .017 and P � .025, respectively); the GJ
asured
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in the G
J and BT groups (P � .023 and P � .003, respectively); the value.045).
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173BONE-TENDON ALLOGRAFT FOR ROTATOR CUFF TEARS
humerus was secured in a custom-designed jig, and thescapula was attached to the test machine ram by use of ajaw clamp to allow for tensile loading along the anatomicvector of IST contraction. Three optical markers weremounted at standardized anatomic locations: (1) at theIST tendon-muscle junction, (2) on the IST midwaybetween the tendon-muscle and bone-tendon repair/insertion sites, and (3) on the proximal humerus im-mediately distal to the bone-tendon repair/insertionsite. Elongation of the repair sites was defined as thechange in distance between markers and was mea-sured to 0.01-mm resolution with an optical trackingsystem (Optotrak; NDI, Waterloo, Ontario, Canada),synchronized with measurement of the applied tensileload. Stiffness was calculated by use of the gradient ofthe respective force/displacement curves. The ISTswere loaded in tension at 0.01 mm/s to a maximumload of 50 N (walking load for a dog)27 or an elonga-ion of 2 mm or greater of either the bone-tendon orendon-muscle junction, whichever occurred first.
FIGURE 4. Radiographs, MRIcans, and gross images ofhoulders in each treatmentroup at 6 months after surgeryor chronic retracted tear.
tiffness and elongation of the operated specimens t
ere compared with the normal contralateral shoul-ers for a control.After biomechanical testing, all specimens were
laced in 10% buffered formalin. After fixing, theumerus-tendon-muscle complex was trimmed into 3ones: (1) humeral tuberosity–tendon, (2) tendon, and3) tendon-muscle. Humeral tuberosity–tendon speci-ens were then placed in a hydrochloric acid–based
ecalcification solution (Surgipath Decalcifier II; Sur-ipath Medical Industries, Richmond, IL) for 24 to 48ours. After routine histologic processing, 5-�m-thickongitudinal sections were cut and stained with H&Eor histologic examination. These sections were sub-ectively assessed with light and polarized-light mi-roscopy by a board-certified veterinary pathologistho was blinded to treatment.
tatistical Analyses
Lameness scores were assessed with a rank sum
est. IST insertion-to-marker distances and biome-
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174 M. J. SMITH ET AL.
chanical data for stiffness and elongation at the re-spective junctions for all groups were assessed by useof a 1-way analysis of variance. Analyses were per-formed with a computer software program (Sigma-Stat; Systat Software, San Jose, CA). P � .05 wasregarded as statistically significant.
RESULTS
Retraction of the IST was noted on all post-releaseradiographs, and degree of retraction was not statisti-cally significant. All dogs showed normal gait at thestart of the study, and all dogs showed mild, visiblelameness (grade 1/2 of 5) 3 weeks after IST release.Six months after treatment, the degree of lamenesswas 1.6 � 0.6 for D dogs, 1.4 � 0.6 for GJ dogs, and0.4 � 0.5 for BT dogs, with BT dogs significantly(P � .01) less lame than the other groups. Lamenessscores are a common functional outcome in dogs thathave been validated using force plate weight bear-ing.28,29 Scores are calculated based on independentbservation of walking and trotting during a dailyxercise protocol. Scores are calculated as 0, no de-ectable lameness; 1, mild weight-bearing lameness; 2,oderate weight-bearing lameness; 3, marked weight-
earing lameness; or 4, non–weight-bearing lameness.Radiographic analysis of markers immediately after
epair showed that retraction was greater in D dogshan in GJ and BT dogs (P � .017 and P � .025,espectively) with no significant difference betweenJ and BT dogs. Six-month analysis showed retrac-
ion in D dogs to be significantly greater than that inoth GJ and BT dogs (P � .023 and P � .003,espectively) and significantly greater in GJ dogs thann BT dogs (P � .045) (Table 1).
Subjective ultrasonographic, MRI, and gross assess-ents of IST integrity and healing at 6 months after
epair indicated that all BT repairs had good bone-one healing with superior bone-tendon, tendon, andendon-muscle integrity when compared with D andJ repairs (Fig 4).Biomechanical testing of the IST bone-tendon-uscle complex with optical tracking to determine
longation and tensile loading at 0.10 mm/s to aaximum load of 50 N (walking load for a dog) or
n elongation of 2 mm showed that all repairs hadignificantly lower stiffness (P � .04) than normalontrols (Fig 5A), whereas the D group had signif-cantly (P � .05) more elongation than the otherroups (Fig 5B). Of the 3 treatment groups, BTepairs had stiffness and elongation characteristics
hat most closely matched normal controls. Histo- mogically, the GJ group was associated with lym-hoplasmacytic infiltrates along the periphery of therafts, tendon degeneration and hypocellularity, andack of any definitive tendon-bone integration (dis-rganized fibrous tissue only) (Fig 6A). The Droup showed evidence of mild to moderate syno-itis/synovial hyperplasia of the joint capsule andisorganized fibrous tissue formation at the area ofebridement, tendon degeneration, and lack of anyefinitive tendon-bone integration (Fig 6B). The BTroup showed complete incorporation of allograftone blocks into host bone, normal bone-tendonunctions, and well-integrated allograft tendon, withlight hypercellularity and hyperplasia and focalnflammation (Fig 6C).
DISCUSSION
The results of this study support those from ourreviously reported work showing that our bone-endon allograft repair method re-establishes aunctional bone-tendon-muscle unit. We showedlearly that integrity of the original repair (based onadiopaque marker location) was maintained only inhe bone-tendon allograft group. Ultrasonographic,
FIGURE 5. Stiffness (A) and elongation (B) of IST bone-tendon-
uscle units for treatment groups and normal controls.
175BONE-TENDON ALLOGRAFT FOR ROTATOR CUFF TEARS
radiographic, MRI, biomechanical, and histologic dataprovided further evidence showing incorporation ofallograft bone, tendon-muscle healing, maintenance oftissue architecture and material properties, biocompat-ibility, and safety.
In addition, the use of the chronic retracted ten-don model with radiographic markers, as opposed tostudies using acute transection or resection models,which do not assess for tendon healing versus newtissue proliferation, more closely mimics the humansituation and provides data regarding the potentialfor clinical applicability. Therefore the evidence forsafety and efficacy of the bone-tendon allograft
technique seen in this chronic retracted IST caninemodel in comparison with 2 standard-of-care treat-ments does have translational clinical applicability.
Historically, treatments for irreparable rotator cufftears have had mixed results. Debridement alone hasbeen shown to be effective in elderly, low-demandpatients when considered in the short-term. Strengthgenerally does not change after surgery, but patient-reported outcome measures, especially for pain, canbe improved. However, several studies have notshown a significant benefit or have shown only modestimprovement. The addition of a tenotomy of the longhead of the biceps may also be beneficial in midtermfollow-up. Whereas Constant scores and patient satis-
GURE 6. Histologic appearance of bone and tendontreatment groups at 6 months after surgery for
atment of chronic retracted IST tear. (A) Directpair with suture bridge and GraftJacket, (B) debride-ent, and (C) bone-tendon allograft reconstruction.&E stain, original magnification 4�.)
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176 M. J. SMITH ET AL.
arthrosis and narrowing of the acromiohumeral dis-tance progressed with time.30
Additional small series have also shown advantagesto partial repair of the infraspinatus to bone. In gen-eral, patients gained elevation and were satisfied withthe procedure; however, overhead use was limitedbecause of weakness.31 Recently, alternative solu-tions, especially for younger patients, have shownpromise. Snyder and colleagues4 reported good toxcellent results in 75% of cases in a series of 16atients and showed improvement in pain and func-ion in a select group of active patients with irrepara-le cuff tears. However, 3 patients had complete fail-re of the graft, and at a mean 26.8-month follow-up,nly 12 patients could place a 1-lb weight on a shelf.he authors believed that increasing ability with timeas a result of graft incorporation rather than im-roved deltoid accommodation. It is our hope that anxcellent reconstruction with a functioning allograftould restore strength and significant overhead
trength early, as well as over time. A solid, function-ng muscle-tendon-bone unit would better restorehoulder mechanics as soon as healing, incorporation,nd early rehabilitation are complete.
All factors considered, we believe it is importanto use the strongest construct possible to bridge aefect. The bone-tendon graft showed much lesseformation than the GraftJacket. This was trueith physiologic load as well as explanted biome-
hanical testing. This is likely because of the elasticodulus of tendon compared with the extracellularatrix, which is an order of magnitude greater than
hat of engineered matrices.32,33 As predicted, theGraftJacket showed significant “stretch” under aphysiologic load.
There are limitations to this study. Healthy researchdogs were used, which certainly have inherent differ-ences in rotator cuff anatomy, function, and healingcompared with humans. Although retraction of thetendon was documented in our model and infraspina-tus muscle atrophy was noted, fatty degeneration wasnot seen. In addition, there was only a single 6-monthendpoint at which all outcome measures were per-formed. As such, we cannot directly apply the resultsof this study to the human clinical situation. However,dogs are considered one of the appropriate models fortranslational research on rotator cuff treatments, and a6-month study duration is sufficient for assessingsafety, longevity of the repair, and functional perfor-mance of the repair.18,32 This is especially true con-
idering the weight-bearing function of the forelimbsf dogs, which in many respects provides a worst-casecenario for rotator cuff healing.
CONCLUSIONS
In this study the use of a chronic IST release modelith tendon retraction and comparison to debridement
nd suture repair with a human dermis–derived patchrovide further evidence for the translational potentialf this rotator cuff repair technique. The bone-tendonllograft technique re-establishes a functional ISTone-tendon-muscle unit and maintains integrity ofepair in this model.
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