Natural History of Rotator CuImplications on Management

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nilateral cuff tears, andalmost perfect 10-year7.8 years, respectively.tomatic side, therewas a66 years of age or older. Amore recent population-based studysupported this nding13a quarter of patients older than 60

2 http://dx.doi.org/10.1053/j.oto.2014.11.0061048-6666//& 2015 Elsevier Inc. All rights reserved.

AR051026.Address reprint requests to Jay Keener, MD, CB 8233, 660 S Euclid Ave, St.

Louis, MO 63110. E-mail: keenerj@wustl.edu50% chance of having a cuff tear on the asymptomatic side atdisease progression can be identied, allowing for furtherincremental increase in cuff tearingwithpatients with bilaterally intact cuffs, ubilateral cuff tears demonstrated andistribution and was 48.7, 58.7, and 6In patientswith a cuff tear on the sympSome studies cited in this articles were publications by the author (Keener),

which were funded by a grant from the NIH, USA Grant no. R01

Department of Orthopaedic Surgery, University of Washington, Seattle, WA.oration and the progression of irreversiblemuscle changeswithtime. Through natural history studies, tears with higher risk of

et al performed bilateral shoulder ultrasounds on patientspresenting with unilateral shoulder pain, demonstrating an

age. The average age ofonease is prevalent in the aging population andmmon cause of shoulder disability. There isoversy among orthopaedic surgeons on theent of rotator cuff disease, and cliniciansariation in the management of cuff tears.1

uidelines set out by the American Academyrgeons on rotator cuff disease demonstrate ay evidence available to help guide treatmentuff pathology. The work group involved ininical practice guidelines suggested the neednd the epidemiology and demographics ofrotator cuff disease. By studying the naturaltter understand risk factors for tear deteri-

renement of surgical indications and a bettof the risks of nonoperative treatment.

Epidemiology of RotatorDiseaseBoth cadaveric2-6 and in vivo imaging studused to dene the prevalence of rotator cuff dsignicant difference in population characterof these studies, the reported prevalencepopulation varies widely. Consistent acronding that increasing age is associatedprevalence of rotator cuff pathology.5,6,10

12KEYWORDS Rotator cuff tear, natural history, surgical indicationsJason Hsu, MD, and Jay D Keener, MD

Degenerative rotator cuff disease is comasymptomatic. The factors related to tear pbeing dened through longitudinal naturalservatively treated painful cuff tears or asyintervals show slow progression of tear enThese studies have highlighted greater risks fas the presence of a full-thickness tear and itendon. Coupling the knowledge of the natuwith variables associated with greater likesurgery will allow better renement of surgicnatural history studies may better dene thearticle reviews pertinent literature regardingon variables important to dening approindications.Oper Tech Orthop 25:2-9 C 2015 Elsevier In l rights reserved.ff Disease and

ly associated with ageing and is oftenssion and pain development are just nowry studies. Most studies that follow con-matic tears that are monitored at regularment and muscle degeneration over time.seaseprogression for certain variables, suchement of the anterior aspect supraspinatusistory of degenerative cuff tear progressiond of successful tendon healing followingications for rotator cuff disease. In addition,s of nonoperative treatment over time. Thisnerative rotator cuff disease with emphasis

multifactorial and includes biological and mechanical inuen-

recommended to perform an early repair for acute, traumatic

inuence the disease progression. Painful tears are often treatedwith physiotherapy, injections, or surgery, any of which maydisrupt the true natural history of disease progression. An idealcohort for dening the risks of tear enlargement and pro-gression of muscle degeneration comprises patients withasymptomatic degenerative cuff tears that can be identiedearly and followed longitudinally. As cuff disease if oftenbilateral, screening subjects with unilateral painful cuff diseaseon presentation can identify a large number of asymptomatictears.12 Additionally, patients with unilateral symptomaticrotator cuff tears have been shown to be at risk for paindevelopment and tear progression on the asymptomaticside.20,26

Tear Initiation and LocationUnderstanding the common locations and site of initiation of

3rotator cuff tears, particularly in young individuals, to optimizethe tissue quality and healing environment, aswell as to preventtear retraction and fatty degeneration of the involved muscle.Bassett and Coeld22 studied 37 patients who had rotator cuffrepair within 3 months of injury and divided them into groupsthat had surgery within 3 weeks, between 3 and 6 weeks, andbetween 6 and12weeks. Thosewhounderwent repairwithin 3weeks had the best functional results. The threshold of thetiming for optimal results of acute cuff tears ranged anywherefrom 3 weeks22-24 to 4 months.25

Treatment of atraumatic degenerative rotator cuff tears thatoccur with advancing age is more controversial. Many factorsincluding patient age, tear size, tendon retraction, muscledegeneration, and overall healing capacity must be taken intoaccount. Study of the natural history of degenerative tears canelucidate the risk factors for tear progression and irreversiblechanges and canhelp cliniciansmake evidence-based decisionsregarding management of these tears.

Study of the Natural History ofRotator Cuff Disease ThroughAsymptomatic Tearsces, recent studies have also suggested a strong genetic inuenceon disease development.16-18 Tashjian et al17 used the UtahPopulation Database to analyze potential heritable predisposi-tion to rotator cuff disease and found signicantly elevated risksin rst- and second-degree relatives of patients with rotator cuffdisease. Harvie et al16 performed ultrasounds in siblings ofmore than 200 patients with full-thickness cuff tears. Using thesubjects spouse as a control group, there was a signicantlyincreased risk for rotator cuff tears in siblings of patients. Asubsequent study by the same group implied that geneticfactors may have a role in the progression of tears as well.18

Another consistent nding throughout the literature is therelatively high prevalence of asymptomatic tears.7,10-12,14,19-21

Because these patients have no pain, have acceptable shoulderfunction, and do not require any treatment for their tears,prospective evaluation of these shoulders has provided us witha wealth of information regarding the natural history of rotatorcuff disease.

Traumatic vs DegenerativeRotator Cuff Tears.Evaluation of a patient should attempt to differentiate traumaticfrom degenerative, attritional rotator cuff tears. Although thesupporting literature is limited to case series,22-25 it is generallyyears and one-half of patients older than 80 years were foundto have a rotator cuff tear. These and other studies14,15 suggestthat tendon degeneration occurs with aging.Although most would agree that rotator cuff disease is

Rotator cuff diseaseAttempting to dene the natural history of rotator cuff diseaseof painful cuff tears is not ideal, as treatment may interrupt ordegenerative rotator cuff tears is essential to describe thepathogenesis of the disease. Early theories on tear initiationreported that the common location of degenerative tears wasthe articular aspect of the anterior supraspinatus adjacent to thebiceps tendon.2,27,28 Tears were felt to then propagate poste-riorly into the supraspinatus and infraspinatus tendons. Thisconventional theory has been challenged with recent research.Kim et al29mapped the common locations of degenerative cufftears with ultrasound by measuring the distance from theanterior tear edge to the biceps tendon and then factoring inthe size (sagittal planewidth) of the tear (Fig. 1). Analyzing datafrom 272 patients, histograms were generated plotting thefrequency of tear involvement within the cuff footprint at eachmillimeter distance posterior from the biceps tendon. Whenanalyzing full-thickness tears, the area approximately13-17 mm posterior to the biceps tendon was most frequentlyinvolved, with only 30% of tears involving the most anterioraspect of the supraspinatus. In addition, when looking at onlysmall full-thickness tears, a similar distribution was foundwiththe highest frequency located 15 mm posterior to the biceps.Figure 1 Ultrasound can be used to measure the distance from theposterior biceps to the anterior border of the rotator cuff tear.

The similarity in tear location of full-thickness tears of varioussizes suggest the common location of tear initiation fordegenerative cuff tears to lie within the rotator crescent, usuallysparing the anterior cable attachment of the supraspinatustendon.This nding had a number of implications based on the

anatomy of the rotator cuff. First, the area 15 mm posterior tothe biceps tendon lies either at the junction of the supra-spinatus and the infraspinatus or predominantly within theanterior infraspinatus, depending on which anatomical de-nition is used.30,31 Second, this area correlates to the middle ofthe rotator crescent tissue as described by Burkhart et al32

(Fig. 2). As opposed to the rotator cable, which is a thickerband of rotator cuff tissue spanning from the anterior supra-spinatus to the posterior infraspinatus, the crescent tissue isthinner, more avascular tissue lateral to the cable. This crescenttissue is typically shielded from stress owing to the suspensionbridge conguration of the cable. These data would suggestthat rotator cuff tears initiate toward themiddle of this crescenttissue and likely propagate anteriorly and posteriorly fromthat point.

importance of the anterior supraspinatus tissue. Ultrasound

nonoperatively.

previous basic science research.

4TearCharacteristics andMuscleDegenerationMuscle degeneration has important prognostic considerationfor patients undergoing rotator cuff repair surgery asadvanced degeneration has been linked to lower rates oftendon healing.33,34 Based on the suspension bridge con-cept, the anterior portion of the supraspinatus is a criticalarea of tissue for distribution of forces along the cable.Disruption of the anterior cable may lead to acceleratedretraction and muscle degeneration. Kim et al35 used similarmethods to the study on tear initiation to quantify theFigure 2 Rotator cuff tears initiate approximately 15 mm posterior tobiceps tendon within the rotator crescent tissue.Tear Enlargement and Pain Development ofAsymptomatic TearsPerhaps the most valuable aspect of studying asymptomaticrotator cuff tears longitudinally is dening the risks of tearprogression and pain development over time. Characterizingthe risks of pain development, tear enlargement, and muscledegeneration can help us rene surgical indications andcounsel patients regarding the risk of nonoperative treatment.This requires long-term prospective studies following theseasymptomatic tears.14,20,26

Moosmayer et al20 followed 50 patients with asymptomatictears over 3-year period. Of 50 tears, 18 (36%) developedsymptoms, and tear progression was signicantly larger in thesymptomatic than the asymptomatic group. Progression ofmuscle atrophy and fatty degeneration was also higher in thesymptomatic group than the asymptomatic group. This studydemonstrated an association between symptom developmentTear Size and Glenohumeral KinematicsAs rotator cuff tears increase in size, disruption of normalglenohumeral kinematics can occur. This may manifest asproximal humeral migration. The effect of rotator cuff size onglenohumeral kinematics and proximal humeral migrationwas investigated by Keener et al36 using a computer-basedcalculation of the humeral head center in relation to the glenoidcenter. A cohort of 98 asymptomatic and 62 symptomatic full-thickness tears was examined. Symptomatic tears and largertears involving the infraspinatus hadmoremigration than tearsin asymptomatic patients and smaller tears isolated to thesupraspinatus. A critical tear area of 175 mm2 was associatedwith proximal humeral migration correlating with a tear size ofapproximately 15 mm with retraction of 12-15 mm. Thesendings highlight the importance of the infraspinatus inmaintaining normal coronal plane kinematics as noted by

37-39was used to measure tear location referenced to the bicepstendon and tear size compared with the degree of fattydegeneration of the cuff muscles. Both tear size and tearlocation were associated with patterns of fatty muscledegeneration. Tears with disruption of the anterior supra-spinatus tendon demonstrated more advanced degenerationof the supraspinatus tendon. Infraspinatus degeneration wasmore closely linked to the sagittal plane size of the tear.Larger tears with propagation into the infraspinatus footprintwere more likely to have both supraspinatus and infra-spinatus muscle degeneration, especially when the anteriorsupraspinatus tendon was compromised (Fig. 3). These datastress the importance of anterior supraspinatus tissue integ-rity. Patientswith cuff tears close to the anteriormargin of thesupraspinatus should be counseled regarding possessing ahigher risk of tendon retraction and muscle atrophy. Closersurveillance of these tears may be warranted when treated

J. Hsu, J.D Keenerand increasing tear size. These results are consistent with thendings of Mall et al26 who investigated variables associated

romwith pain development in asymptomatic tears, also noting thatpain development in patients with asymptomatic tears wasassociated with tear progression.A subsequent report of this cohort has better dened the

risks of tear progression and pain development for a period of5 years after identication of an asymptomatic degenerativetear.40 A total of 224 patients with 118 full-thickness tears, 56partial-thickness tears, and 50 controls were followed longi-tudinally for a median of 5.1 years. Tear enlargement occurredin a time-dependent manner with greater risks of enlargementseen in more severe tear types. Tear progression or enlarge-ment was seen in 49% of shoulders, with a median time toenlargement of 2.8 years. Full-thickness tears were 1.5 and4 times more likely to enlarge compared with partial-thicknesstears and control shoulders. Likewise, muscle degenerationwas more frequent in full-thickness tears and those tears thatprogressed in size. Overall, 46% of shoulders developed newpain, and the median time to pain development was 2.6 years.Tear enlargement was a signicant risk factor for pain develop-ment. Thirtyeight percent of shoulders that remained asymp-tomatic enlarged compared to 63% of shoulders thatdeveloped pain. More severe tear types (full vs partial) also

Figure 3 Association between location of tear (distance fdegeneration.Rotator cuff diseasehad a greater risk for future pain development. The ndingsfrom this study support the progressive nature of degenerativerotator cuff disease and highlight full-thickness tears to be ahigher risk group for future tear enlargement, progression ofmuscle degeneration, and pain development.

Natural History of SymptomaticRotator Cuff TearsCurrently, few studies have evaluated the natural history ofsymptomatic rotator cuff tears.41-43 Maman et al43 retrospec-tively studied 59 shoulders with full- and partial-thicknessrotator cuff tears treated nonoperatively. Each shoulder had abaseline magnetic resonance imaging and a repeat imagingperformed a minimum of 6 months later. Progression of tearsize was found in 48% of the tears that were followed for atleast 18months vs only 19% of those followed for less than 18months. Full-thickness tears were more likely to progress thanpartial-thickness tears (52% vs 8%). Age was an importantpredictor of tear deterioration, with 54% of tears in patientsolder than 60 years progressing vs only 17% of tears in thoseyounger than 60 years. Safran et al42 specically investigated acohort of patients younger than 60 years who were treatednonoperatively for full-thickness rotator cuff tears and found ahigher rate of tear progression in these younger patients. Of the61 tears, 49% of tears increased in size by ultrasound. Therewas a signicant correlation between pain and increase intear size.Fucentese et al41 reported seemingly contradictory ndings

in their report of 24 patients refusing operative treatment forfull-thickness supraspinatus tears. They used magnetic reso-nance (MR) arthrography as their initial imaging modality andMR without arthrography for their follow-up imaging andreported no increase in the mean size of the rotator cuff tears3.5 years after the initial MR arthrogram. Although the meantear size did not increase, 8 of the 24 patients (33%) had anincrease in tear size, and 4 (17%) had no change in size. Theydo report a high level of satisfaction in this group of patientstreated nonoperatively.The Multicenter Orthopaedic Outcomes Network Shoulder

biceps to anterior margin of tear) and rotator cuff fatty

5Group has also provided valuable information in the non-operative treatment of symptomatic rotator cuff tears.44-47 Thisgroup has done multiple observational and cross-sectionalstudies on more than 400 patients with atraumatic, full-thickness rotator cuff tears. They have found that pain andduration of symptoms are not strongly associated with theseverity of rotator cuff tears45,48 and that nonoperativemanage-ment with physical therapy is effective in treating 75% ofpatients up to 2 years.46 Interestingly, the most importantfactor for predicting a successful response to conservativetreatment from this study was the patients perception thatphysical therapy would be benecial.The association of pain with full-thickness rotator cuff tears

is controversial. Studies by the Multicenter Orthopaedic Out-comes Network Shoulder Group suggest that pain andduration of symptoms do not correlate with the severity ofrotator cuff tears45,48; however, other studies have shownstronger correlations between enlargement of tears and devel-opment of pain.20,26 These differences are likely attributed to

consideration. Prior treatments such as physical therapy,injections, and surgery should be documented.Physical examination is performed with the shoulder

exposed. Atrophy of the spinati fossa can be visually distinctin chronic cuff tears (Fig. 4). The examiner will often notesubacromial crepitus with rotation. Both passive and activerange of motion should be documented to rule out restrictionsin motion due to arthritic conditions or adhesive capsulitis.Internal rotation behind the backmay be limited due to pain inpatients with active cuff inammation. Signs of subacromialimpingement can identify patients with cuff-based pain. Acareful examination for signs of cervical radiculopathy shouldbe performed especially in patients withmedial scapula pain orsymptoms radiating below the elbow.Strength testing can isolate eachof the 4 rotator cuffmuscles.

Resistance to abduction with the thumb down can test thesupraspinatus. External rotation with the arm at the side cantest infraspinatus strength, whereas an external rotation lagsign and the Hornblowers sign can indicate posterior tearextension into the teres minor. The abdominal compressiontest can test subscapularis function. The lift-off test can also testsubscapularis function but is often restricted by pain in patients

J. Hsu, J.D Keener6differences in study design (cross sectional vs prospectiveobservational). More data, other than tear size progression,may identify factors causally related to the onset of pain.

Important Clinical andRadiographic VariablesWhen evaluating a patient with a suspected degenerativerotator cuff tear, a comprehensive history is the rst andarguably the most important aspect of a complex decision-making process. The patients age is thought to be a strongpredictor of rotator cuff healing if operative intervention isconsideredolder patients are less likely to have a durablerepair. Time since initiation of symptoms is important toestimate the chronicity of the tear. While inuencing otherfactors, such as tear size and location, chronicity likely has anundened effect on healing potential. Activity expectationsmust be taken into considerationa patient without highfunctional demands may retain good function with a full-thickness rotator cuff tear. On the contrary, a small full-thickness rotator cuff tear may present difculties to a younglaborer who requires overhead motion and strength. Geneticpredisposition, hand dominance, smoking, medical comor-bidities, and social factors affecting postoperative rehabilitationpotential are other variables that should also be taken into

Figure 4 Atrophy of the supraspinatus and infraspinatus fossas can bevisible in chronic tears.with tears of the superior cuff. External rotation weakness withor without abduction weakness out of proportion to theseverity of a cuff tear may be secondary to pain but also maysignal a suprascapular nerve injury. Consideration for electro-myographic or nerve conduction studies should be entertainedin these select cases.Imaging should begin with plain radiographs including AP,

true AP (Grashey view) in 301 of abduction, scapular Y, andaxillary views. The Grashey view activates the deltoid muscleallowing proximal humeral migration in chronic, larger tears(Fig. 5). The scapular Y view can assess acromial spursFigure 5 Proximal humeral migration is best viewed on a true APradiograph with the arm in 301 of abduction. AP, anteroposterior.

associated with cuff tears that may need to be addressed at thetime of surgery.49 The axillary view demonstrates joint spacenarrowing as well as potential anterior or posterior humeralsubluxation.Advanced imaging modalities including ultrasound and

MRI should be used when a rotator cuff disease is suspectedby history and examination. These modalities can be used tofurther characterize the size, location, and retraction of rotatorcuff tears. The presence or absence of muscle atrophy shouldbe documented in full-thickness tears (Fig. 6) and gradedaccording to the Goutallier classication.50 Concomitantpathology to other structures such as the long head of thebiceps, labrum, and early glenoid and humeral chondrosisshould be assessed.

Clinical Decision MakingOur understanding of the natural history of rotator cuff diseasecontinues to improve, and it assists clinicians in an oftencomplex decision-making process. As we continue to learnmore, our indications for operative repair will continue to be

associated with muscle degeneration, early surgical intervention

Rotator cuff diseaseFigure 6 Fatty muscle degeneration of the rotator cuff muscle bellies isrened. Surgical indications may be simplied by dividing cufftears into 3 categories where the risks for nonoperativetreatment may vary signicantly and the potential benets ofsurgery may be maximized.Group IEarly operative repair. Early surgery should be

considered in patients presenting with a rotator cuff tearstemming from a distinct, acute event with imaging thatcorroborates an acute injury. Pain or weakness before injuryand signs ofmuscle degeneration on imagingmay be signs of anacute-on-chronic tear. In these situations, an injury resulting in asignicant increase in shoulder weakness likely represents asignicant acute component to the tear. Consideration for earlybest visualized on MRI with T1 oblique sagittal cuts. MRI, magneticresonance imaging.or close surveillance should be employed in patients who havefull-thickness tears involving the anterior supraspinatus tendon.Group IITrial of conservative treatment. Initial nonoper-

ative treatment is reasonable in any patient with a painfulpartial-thickness tear or a potentially reparable full-thicknesstear that is not acute in onset. In these cases, conservativetreatment has been shown to produce reliable results in theshort term, and some signs of tear chronicity are often alreadyevident. Although risks for tear enlargement and muscleatrophy progression are present, the natural history studiessuggest that these changes occur slowly allowing for adequatetime to attempt conservative treatment. Surgery can beconsidered if conservative treatment fails.Group IIIMaximize conservative treatment. Conservative

treatment should be maximized in patients in situations wheresuccessful tendon healing is unlikely. These include olderpatients (465-70 years), patients with chronic full-thicknesstears (retracted tears of any size with advanced muscledegeneration), and tears associated with xed proximalhumeral migration (signs of chronic mechanical contact ofthe greater tuberosity and acromion).

ConclusionsOur understanding of the natural history of rotator cuff diseasecontinues to expand. Following asymptomatic rotator cufftears found in patients with symptomatic contralateral should-ers is a good model for studying the natural history. Using thismodel, important information regarding tear initiation, loca-tion, size, progression, and survivorship has been gathered.Degenerative tears initiate approximately 15 mm posterior tothe biceps tendon, with less than one-third of tears involvingthe anterior edge of the supraspinatus tendon. Loss of integrityof the anterior supraspinatus tissue is associated with supra-spinatus muscle degeneration. A critical tear size of approx-imately 175 mm2 is associated with early disruption of normalkinematics of the shoulder. Approximately 50% of degener-ative tears will progress in size by 5 years, and full-thicknesssurgery should be given in these scenarios if the imaging tests donot suggest severe muscle atrophy. Early repair should beperformed in acute subscapularis tears or more chronicsubscapularis tears with biceps tendon instability. Acute,retracted subscapularis tears are considered more urgent owingto the potential forxed retraction andmuscle degeneration thatcan accompany these injuries. Early operative repair should alsobe considered in small- to medium-sized full-thickness degen-erative tears in patients younger than 62-65 years with minimalor no muscle atrophy; however, specic patient characteristicsshould be used to rene which patients should be indicated forrepair. The reason to consider early surgery in these scenariosrelates to the established risks for the potential for tear enlarge-ment and progression of muscle atrophy in patients who stillpossess a reasonable potential to heal a surgical repair. Owing tothe fact that loss of anterior supraspinatus tissue integrity is

7tears are more likely to enlarge and develop muscle degener-ation than partial-thickness tears. Aswe continue to learnmore

about the natural history of cuff disease through this model,clinicians will be able to further rene indications for rotatorcuff repair.

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Rotator cuff disease 9

Natural History of Rotator Cuff Disease and Implications on ManagementIntroductionEpidemiology of Rotator Cuff DiseaseTraumatic vs Degenerative Rotator Cuff TearsStudy of the Natural History of Rotator Cuff Disease Through Asymptomatic TearsTear Initiation and LocationTear Characteristics and Muscle DegenerationTear Size and Glenohumeral KinematicsTear Enlargement and Pain Development of Asymptomatic Tears

Natural History of Symptomatic Rotator Cuff TearsImportant Clinical and Radiographic VariablesClinical Decision MakingConclusionsReferences