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Correspondence

Displaced Clavicle Fractures in


Adolescents: Facts, Controversies,
and Current Trends
To the Editor: As members of the III studies to formulate recommen-
American Academy of Orthopaedic dations when these provide the best
Surgeons (AAOS) Council on Re- evidence available. Although point-
search and Quality, we read with ing out that no level I or II studies
great interest the correspondence have been published on the subject
between Dr. Rickert1 and Drs. Ho- of nonsurgical management of clav-
salkar, Pandya, and Namdari2 icle fractures may be true, Dr. Ho-
concerning the article “Displaced salkar and coauthors imply that
Clavicle Fractures in Adolescents: level I and II studies are the only
Facts, Controversies, and Current studies that the AAOS uses to gen-
Trends.”3 When it comes to dis- erate clinical practice guidelines
cussing evidence-based practice, recommendations. Inaccurate state-
unintentional misuse of language ments such as this can lead to mis-
can misinform the reader; thus, we perceptions about AAOS guidelines
feel obliged to comment. and ultimately undermine their
Dr. Rickert’s criticism that value to the end user.
Dr. Hosalkar and his colleagues The AAOS should be proud of
present “no evidence whatsoever” the work done by its many volun-
might more appropriately be stated teers and staff to develop and im-
as presenting evidence comprised prove the process for creating
Dr. Goldberg or an immediate family only of individual studies. It does evidence-based CPGs. We invite
member serves as a board member, not appear that the authors either Dr. Rickert, Dr. Holsakar and his
owner, officer, or committee member
of the American Academy of
systematically evaluated the litera- coauthors, and other readers of the
Orthopaedic Surgeons. Dr. Jevsevar ture or based their position on mul- Journal of the American Academy
or an immediate family member is a tiple evidence data points akin to of Orthopaedic Surgeons to learn
member of a speakers’ bureau or
treatment recommendations found more about AAOS Clinical Practice
has made paid presentations on
behalf of Medacta USA; has stock in evidence-based clinical practice Guidelines by logging on to http://
or stock options held in OMNIlife guidelines. www.aaos.org/guidelines.
science; and has received research Dr. Hosalkar’s claim that “[f]rom
or institutional support from Medacta
USA. Dr. Bozic or an immediate the perspective of AAOS guidelines, Michael J. Goldberg, MD
family member serves as a board [level III and IV studies] do not meet Rosemont, Illinois
member, owner, officer, or the criteria to be included in any David Jevsevar, MD, MBA
committee member of the American
Academy of Orthopaedic Surgeons,
evidence-based recommendation as St. George, Utah
the American Association of Hip and even modest evidence” clearly mis- Kevin J. Bozic, MD, MBA
Knee Surgeons, American Joint states the process used by the AAOS San Francisco, California
Replacement Registry, the American in developing evidence-based clinical
Orthopaedic Association, California
Joint Replacement Registry Project, practice guidelines. As recommended
the California Orthopaedic by seminal guideline developers in
Association, Harvard Business medicine,4 the AAOS uses the best
References
School, and the Orthopaedic
Research and Education
available evidence to determine the
Foundation. strength of a recommendation (as 1. Rickert JB: Displaced clavicle fractures
in adolescents: Facts, controversies,
http://dx.doi.org/10.5435/
Strong, Moderate, or Limited) in a and current trends. J Am Acad Orthop
JAAOS-21-04-199 guideline and does indeed use level Surg 2013;21(1):1-2.

April 2013, Vol 21, No 4 199


2. Hosalkar H, Pandya N, Namdari S: 3. Pandya NK, Namdari S, Hosalkar HS: 4. Cook DJ, Mulrow CD, Haynes RB:
Facts, controversies, and current trends. Displaced clavicle fractures in Systematic reviews: Synthesis of best
J Am Acad Orthop Surg 2013;21(1):1-2. adolescents: Facts, controversies, and evidence for clinical decisions. Ann
current trends. J Am Acad Orthop Surg Intern Med 1997;126(5):376-380.
2012;20(8):498-505.

200 Journal of the American Academy of Orthopaedic Surgeons


Editorial
Thank You, Adria
Jeffrey S. Fischgrund, MD Publication of the Journal of the keep the editorial board on track,
American Academy of Orthopaedic Adria is at the center of a well-oiled
Surgeons (JAAOS) is a team effort. machine.
With a staff of 13 at the Academy, She has contributed to making
11 Deputy Editors, hundreds of re- JAAOS the leading orthopaedic re-
viewers, and scores of authors, view journal in the world. With a
managing the many personalities circulation of more than 50,000
involved in producing JAAOS ev- copies monthly, the Journal adds to
ery month is an enormous under- the knowledge base of the entire in-
taking. All of these talented pro- ternational orthopaedic commu-
fessionals, however, have one nity. Adria not only has watched us
common link—Adria Landy. grow but is also one of the major
Adria has been the Journal’s Man- reasons why we have grown.
uscript Coordinator during my tenure People often ask me how I find
as Editor-in-Chief (and those of my the time to manage my practice,
predecessors). She was at the Acad- stay connected with friends and
emy before the launch of JAAOS family, and edit JAAOS, all at the
in 1993. Now, after 20 years of ser- same time. My answer is simple:
vice, in which she helped produce 164 talented authors, dedicated editors
issues of the Journal, totaling 1,158 and reviewers, and an Academy
articles, and during which she tire- staff second to none. Adria Landy
lessly assisted 4 Editors-in-Chief and epitomizes the dedication, persever-
22 Deputy Editors, Adria will be re- ance, and talent that make editing
tiring this month. the Journal my most enjoyable job.
What she has accomplished “be- Although any job position can be
hind the scenes” is essential to the filled, people cannot be so easily re-
continuing success of JAAOS. For placed. Adria is that unique person
example, every bit of correspon- who has helped the Journal thrive.
dence to authors, reviewers, and She should be extremely proud of
editors either goes to, or comes her accomplishments in assisting
from, this remarkable woman. the Academy as well as the entire
Whether it is a “gentle reminder” orthopaedic community.
Dr. Fischgrund is Editor-in-Chief, to me that my review is late, or list- Thank you, Adria, for all that
Journal of the American Academy of ing every article (by subspecialty) you have done.
Orthopaedic Surgeons, Rosemont, IL. for every Deputy Editor to help You will be missed.
Dr. Fischgrund or an immediate family
member has received royalties from
Stryker; serves as a paid consultant to
Baxter, Medtronic, Relievant, Smith &
Nephew, Stryker, and TranS1; has
stock or stock options held in TranS1
and Understand.com; has received
research or institutional support from
Smith & Nephew and Stryker; and
serves as a board member, owner,
officer, or committee member of the
Cervical Spine Research Society and
the Lumbar Spine Research Society.
http://dx.doi.org/10.5435/
JAAOS-21-04-201

April 2013, Vol 21, No 4 201


Guest Editorial
Update on Surgery of the Hand
Steven Z. Glickel, MD Changes in surgical disciplines are time periods. Also, the procedure
characteristically subtle and evolu- can be repeated with good results.3
tionary, not dramatic and revolu- One of the great advantages is that
tionary. Nevertheless, some areas in postoperative rehabilitation is
hand surgery have recently seen de- rarely needed.
velopments that have modified Clostridial collagenase was ap-
practice substantially. These include proved in 2010 by the US FDA for
developments for the treatment of use in treating Dupuytren disease.
Dupuytren disease, the use of nerve It is injected into palmar and digital
transfer for nerve reconstruction, cords, followed by manipulation of
and hand allotransplantation, par- the finger straight on the day of or
ticularly for bilateral upper extrem- within a few days after injection. In
ity amputees. The magnitude of the a level I study, 88.9% of MCP
impact of these modalities, in terms joints and 57.7% of PIP joints with
of the number of patients and sur- a baseline contracture of ≤50° were
geons affected, ranges from broad reduced to zero degrees to 5° of ex-
(Dupuytren disease) to almost min- tension after collagenase treatment
iscule (hand transplantation). with one to three injections per
Traditionally, the treatment of Du- cord.4 Recurrence at 3 years in fully
puytren contracture of >30° at the corrected joints was 27% for MCP
metacarpophalangeal (MCP) joint and 56% for PIP joints.5
and of 10° to 15° at the proximal in- Until recently, reconstruction for
terphalangeal (PIP) joint has been by complex nerve pathology such as
partial palmar and digital fasciectomy brachial plexus palsy typically in-
with or without skin graft, depending volved bridging gaps in nerves with
on the extent of fasciodermal involve- autogenous nerve grafts supple-
ment and whether the disease is pri- mented with tendon reconstruction.
mary or recurrent. Two recent treat- Currently, reconstruction preferen-
ment techniques have substantially tially includes nerve transfer of ex-
altered the way many hand surgeons pendable nerves or parts thereof to
approach Dupuytren contracture. In restore motor and sensory function.
needle aponeurotomy, the dermis is lo- Examples of transfers include the
cally anesthetized, and the palmar and triceps motor branch to the axillary
digital cords are transected using the nerve;6 the ulnar motor fascicle to
tip of a 25-gauge needle as a knife at the biceps motor branch;7 and the
several points along the cord as the spinal accessory nerve to the supra-
finger is manually manipulated scapular nerve, combined with in-
straight. Reported results have been tercostal muscles to the posterior
excellent and complications, few.1,2 deltoid and triceps for shoulder ab-
From the C.V. Starr Hand Surgery
In a series of 1,013 digits, contrac- duction and elbow extension.8 Be-
Center, Columbia University, New York,
NY. tures were corrected to ≤5° in 98% cause these transfers are usually
of MCP joints and 67% of PIP done outside the zone of injury,
Dr. Glickel or an immediate family
member serves as an unpaid consultant joints.2 The reported rate of recur- they obviate or diminish the need
to Tri-Medics and serves as a board rence varies but is approximately for laborious dissection through a
member, owner, officer, or committee 10% higher (50% versus 40%) for scarred plexus. Nerve transfers are
member of the Dupuytren Foundation.
aponeurotomy compared with increasingly being used for periph-
http://dx.doi.org/10.5435/ open fasciectomy for equivalent eral reconstruction, as well, such as
JAAOS-21-04-202

202 Journal of the American Academy of Orthopaedic Surgeons


to enhance motor function of the ul- include proximal polyethylene-on- 5. Peimer CA, Blazar P, Coleman S, et al:
Dupuytren contracture recurrence
nar nerve by distal transfer of the metal components press-fit into the ra- following treatment with collagenase
branch of the anterior interosseous dius and a distal component press-fit clostridium histolyticum (CORDLESS
nerve to the pronator quadratus study): 3-year data. J Hand Surg Am
and supplemented with screws into the 2013;38(1):12-22.
muscle, which is expendable. This carpus and metacarpals. Pain relief is
6. Lee JY, Kircher MF, Spinner RJ, Bishop
type of transfer can also be used end- generally very good, from 8.0 to 2.2 in AT, Shin AY: Factors affecting outcome
to-side to “supercharge” a nerve a recent series.14 The complication of triceps motor branch transfer for
grafted more proximally.9 isolated axillary nerve injury. J Hand
rate remains unacceptably high, Surg Am 2012;37(11):2350-2356.
Another development in nerve re- however, and in a medium-term 7. Siqueira MG, Socolovsky M, Heise CO,
construction is the use of decellular- follow-up study, the reoperation rate Martins RS, Di Masi G: Efficacy and
ized nerve allograft to bridge large was 50%.15 Joint arthroplasty of the safety of Oberlin’s procedure in the
treatment of brachial plexus birth palsy.
nerve gaps without incurring the do- PIP joint remains a challenge. Silastic Neurosurgery 2012;71(6):1156-1160,
nor site morbidity of harvesting au- implants have remained essentially discussion 1161.
tograft, as with the sural nerve. Re- unchanged for three decades. They 8. Malungpaishrope K, Leechavengvongs S,
cent studies have confirmed the provide pain relief and limited range Witoonchart K, Uerpairojkit C, Boony-
alapa A, Janesaksrisakul D:
efficacy of allograft, and the results of motion. The early complication Simultaneous intercostal nerve transfers
are comparable to those of historical rate is low, but the longevity of the to deltoid and triceps muscle through the
controls of autograft; however, no posterior approach. J Hand Surg Am
implants is limited by the material 2012;37(4):677-682.
direct comparison has been done.10 properties of the Silastic, with defor-
9. Barbour J, Yee A, Kahn LC, Mackinnon
Hand transplantation has been con- mity and fracture of the prosthesis. SE: Supercharged end-to-side anterior
troversial since the first single hand More recent prosthetic designs have interosseous to ulnar motor nerve
transfer for intrinsic musculature
transplant 14 years ago. Functional re- used pyrocarbon- or polyethylene- reinnervation. J Hand Surg Am 2012;
sults of early procedures were fair and on-metal materials in a design that 37(10):2150-2159.
raised the ethical question of whether more nearly recapitulates normal 10. Cho MS, Rinker BD, Weber RV, et al:
it is reasonable to expose a patient to anatomy than the Silastic hinged de- Functional outcome following nerve
repair in the upper extremity using
the risk of chronic immunosuppression sign. However, these implants have a processed nerve allograft. J Hand Surg
for a single hand that will likely func- high complication rate, as well. A re- Am 2012;37(11):2340-2349.
tion only moderately well. That argu- cent study comparing the three main 11. Shores JT, Imbriglia JE, Lee WP: The
ment becomes somewhat less compel- types of prostheses showed that re- current state of hand transplantation.
J Hand Surg Am 2011;36(11):1862-
ling in discussing patients with bilateral sults were comparable but the com- 1867.
hand amputations for whom the psy- plication rates of the pyrocarbon-on-
12. Ravindra K, Haeberle M, Levin LS, Ild-
chological and functional advantages of metal and polyethylene-on-metal stad ST: Immunology of vascularized
hand transplantation may well out- implants were significantly higher composite allotransplantation: A primer
for hand surgeons. J Hand Surg Am
weigh the risk.11 Immunosuppression is than those of the Silastic implant.16 2012;37(4):842-850.
shifting from traditional corticosteroid,
13. Chung KC, Oda T, Saddawi-Konefka D,
calcineurin inhibitor (ie, tacrolimus, cy- Shauver MJ: An economic analysis of
closporine), and antimetabolite drugs References hand transplantation in the United
States. Plast Reconstr Surg 2010;125(2):
to induction agents (eg, polyclonal an-
589-598.
tilymphocyte globulins, alemtuzumab) 1. Eaton C: Percutaneous fasciotomy for
Dupuytren’s contracture. J Hand Surg 14. Nydick JA, Greenberg SM, Stone JD,
and monoclonal antibodies (eg, basi- Williams B, Polikandriotis JA, Hess AV:
Am 2011;36(5):910-915.
liximab, daclizumab). Interest is in- Clinical outcomes of total wrist
2. Pess GM, Pess RM, Pess RA: Results of arthroplasty. J Hand Surg Am 2012;
creasing in techniques of immunomod-
needle aponeurotomy for Dupuytren 37(8):1580-1584.
ulation in which tolerance is induced in contracture in over 1,000 fingers. J Hand
Surg Am 2012;37(4):651-656. 15. Ward CM, Kuhl T, Adams BD: Five to
the recipient by infusion of host mar- ten-year outcomes of the Universal total
row.12 The cost-effectiveness of hand 3. van Rijssen AL, Werker PM: wrist arthroplasty in patients with
transplantation remains a challeng- Percutaneous needle fasciotomy for rheumatoid arthritis. J Bone Joint Surg
recurrent Dupuytren disease. J Hand Am 2011;93(10):914-919.
ing dilemma.13 Surg Am 2012;37(9):1820-1823.
16. Daecke W, Kaszap B, Martini AK, Ha-
Arthroplasty in the wrist and hand 4. Hurst LC, Badalamente MA, Hentz VR, gena FW, Rieck B, Jung M: A prospec-
lags behind the level of sophistication et al; CORD I Study Group: Injectable tive, randomized comparison of 3 types
collagenase clostridium histolyticum for of proximal interphalangeal joint arthro-
and success achieved in the lower ex- Dupuytren’s contracture. N Engl J Med plasty. J Hand Surg Am 2012;37(9):
tremity. Current total wrist prostheses 2009;361(10):968-979. 1770-1779, e1-e3.

April 2013, Vol 21, No 4 203


Review Article

Meniscal Repair

Abstract
Catherine Laible, MD Historically, treatment of meniscus tears consisted of complete
Drew A. Stein, MD meniscectomy. Over the past few decades, however, the long-term
morbidities of meniscal removal, namely the early development of
Daniel N. Kiridly
knee osteoarthritis, have become apparent. Thus, management of
meniscal tears has trended toward meniscal preservation. Recent
technological advances have made repairs of the meniscus easier
and stronger. In addition, adjunctive therapies used to enhance the
healing process have advanced greatly in the past few years.
Today, with increased understanding of the impact of meniscal loss
and the principles of meniscal repair and healing, meniscal
preservation is viewed as an increasingly realistic and important
goal in the management of meniscus tears.

K nee arthroscopy is the most


common type of orthopaedic
surgery performed in the United
proteoglycans (<1%), and elastin
(<1%).
Arnoczky and Warren3 first de-
States, accounting for >900,000 pro- scribed the blood supply for each
cedures in 2006.1 Of these, more meniscus. They illustrated a micro-
than half involved a meniscal tear. vascular perimeniscal plexus sup-
Traditionally, meniscal tears were plied by the vascularized synovial tis-
managed with meniscectomy. How- sue on the periphery of the menisci.
ever, since the long-term morbidities This plexus is formed from the me-
of meniscus removal became appar- dial and lateral geniculate arteries,
ent (eg, early development of knee which are branches of the popliteal
osteoarthritis), management has artery. The vascular supply termi-
been increasingly focused on menis- nates in short capillaries that extend
From the New York University
cal preservation. from the periphery inwards, consti-
Hospital for Joint Diseases, New
York, NY (Dr. Laible and Dr. Stein) tuting approximately 10% to 30%
and the New York University School of the width of the medial meniscus
of Medicine, New York (Mr. Kiridly). Anatomy and 10% to 25% of the width of the
None of the following authors or any lateral meniscus (Figure 1).
The medial and lateral menisci are
immediate family member has
received anything of value from or each approximately 3 cm wide.2 The
has stock or stock options held in a medial meniscus is approximately 4 Meniscal Biomechanics
commercial company or institution to 5 cm in length, and the lateral me-
related directly or indirectly to the
subject of this article: Dr. Laible,
niscus is approximately 3 to 4 cm in The medial and lateral menisci have
Dr. Stein, and Mr. Kiridly. length. The normal meniscus is com- important biomechanical functions
J Am Acad Orthop Surg 2013;21:
posed of approximately 70% water within the knee joint. These include
204-213 and 30% organic matter. The or- load bearing, shock absorption, joint
ganic matter is made up of approxi- stability, joint lubrication, and pro-
http://dx.doi.org/10.5435/
JAAOS-21-04-204 mately 75% collagen (types I, II, III, prioception.
IV, V, VI, and XVIII) and 25% other In 1948, Fairbank4 examined post-
Copyright 2013 by the American
Academy of Orthopaedic Surgeons. organic matter, including proteogly- meniscectomy knees and noted that
cans (15%), DNA (2%), adhesion over time they developed joint-space

204 Journal of the American Academy of Orthopaedic Surgeons


Catherine Laible, MD, et al

Figure 1 Figure 2

Anterior
C D

B E

0 1 2 3 Medial Lateral 3 2 1 0

Cross-section of the medial


compartment of the knee,
highlighting the meniscal
vasculature. F = femur,
A F
PCP = perimeniscal capillary
plexus, T = tibia. (Reproduced with Posterior
permission from Arnoczky SP,
Warren RF: Microvasculature of the
human meniscus. Am J Sports Schematic diagram of the medial and lateral meniscus demonstrating the 12
Med 1982;10[2]:90-95.) Cooper zones. The radial thirds are labeled with letters A through F, and the
numbers zero through 3 represent the subdivisions into circumferential thirds.
(Adapted with permission from Cooper DE, Arnoczky SP, Warren RF:
Meniscal repair. Clin Sports Med 1991;10[3]:529-548.)

narrowing and femoral condylar


flattening. He was the first to de-
scribe the load-bearing function of 70% and results in an increase in ular surface, thereby assisting lubri-
the meniscus. When an axial load is peak pressures and an increase in the cation.5
applied across the knee joint, the me- area under high pressure.6 More re-
nisci experience tensile, compressive, cent studies have shown that even
and shear stresses.5 Studies measur- small decreases in meniscus volume, Meniscal Tears
ing contact pressures on the tibial such as following a partial lateral
Meniscal tears are described by loca-
plateau have shown that the menisci meniscectomy, can significantly alter
tion and shape. The meniscus can be
transmit at least 50% of the load knee mechanics, resulting in in-
divided into vascular and avascular
placed across the knee joint in the creased peak pressures and mean
zones (eg, red, red-white, white).
first 90° of flexion, with higher contact pressure.8
Cooper et al9 further categorized
transmission at full extension.6 Joint stability is enhanced by the
these into 12 zones, with each menis-
The crescentic wedge shape of the shape of the meniscus and the at-
cus divided into thirds both longitu-
meniscus assists in the translation of taching ligaments. The concavity of dinally and radially (Figure 2).
compressive forces from the articular the superior aspect of the meniscus
Tears of the meniscus can be classi-
cartilage into concentric forces on and the flat surface of the inferior as- fied as acute or degenerative. A de-
the meniscus. These hoop stresses are pect of the meniscus enhance the generative tear occurs in a meniscus
then transmitted to the bony anchors congruity of the tibiofemoral joint. that has been worn down by age,
of the meniscal horns by the circum- The meniscotibial and meniscofemo- chronic knee instability, or malalign-
ferential fibers of the meniscus.7 This ral ligaments also add to the stability ment. Tear types include horizontal;
distribution of force helps protect the of an otherwise incongruous joint. bucket handle; longitudinal (ie, verti-
articular cartilage and prevent de- Although it has been suggested cal); oblique (ie, flap); radial; com-
generation. that the meniscus has a role in joint plex, which consists of a combina-
Loss of meniscal volume has a dra- lubrication, no studies to date have tion of different tear morphologies;
matic impact on the contact mechan- proved a direct contribution. It has and meniscal root (Figure 3). The
ics of the knee joint. Biomechanical been proposed that the conformity of shape, configuration, and location of
studies have shown that complete shape between the meniscus and the a tear are important factors in deter-
medial meniscectomy decreases the femoral condyles allows for a thin mining whether it will heal following
tibiofemoral contact area by 50% to film of fluid to remain over the artic- repair.

April 2013, Vol 21, No 4 205


Meniscal Repair

Figure 3 Table 1
Indications for Meniscal Repair

Tear >1 cm and <4 cm in length


Red-red zone tears
Vertical tears
Patient age <40 y
No mechanical axis malalignment
Acute tears (ie, <6 wk)
Concurrent anterior cruciate ligament
reconstruction

Repair Indications

Schematic illustration of the types of meniscal tears. Note that the bucket- Although meniscal preservation is
handle tear has a morphology similar to that of the longitudinal or vertical important, only certain types of tears
tear but involves more displacement of the tear edges. are amenable to repair. Factors that
contribute to good healing potential
and low failure rates have been well
varus or valgus stress to the knee studied. The relative indications of
Diagnosis while internally or externally rotat- meniscal repair are summarized in
ing the leg. The test is positive when Table 1.
The diagnosis of a meniscal tear is
a pop or a click is palpated at the The vascular supply of a meniscal
typically clinical. Symptoms include
joint line as the knee is slowly ex- tear is the most important intrinsic
joint line tenderness, mechanical
tended. The sensitivity for this test is factor in healing. Most meniscal re-
symptoms of catching or a locking
48% and 65% and the specificity is pairs are attempted on tears that are
sensation, clicking on moving the 94% and 86% for the medial and close to the vasculature supply, that
knee, and intra-articular effusion. lateral menisci, respectively. is, in the red-red or red-white zone.
The clinical evaluation should in- The Thessaly test was described by Prospective studies evaluating clini-
clude assessing for joint line tender- Karachalios et al10 in 2005. The pa- cal and arthroscopic assessments of
ness, range of motion testing, the tient stands on the affected knee and healing have found that tears within
Apley grind test, the McMurray test, flexes it to 20°, then internally and 2 mm of the meniscal vascular rim
and the Thessaly test. Joint line ten- externally rotates the knee and body. have the highest rates of healing fol-
derness has a reported sensitivity of A positive test produces either pain lowing repair.13,14 Conversely, those
71% and 78% and specificity of at the joint line or a locking or catch- that lie >4 mm from the rim have
87% and 90% for medial and lateral ing sensation. The Thessaly test was high rates of failure following re-
meniscal tears, respectively.10 For the found to have sensitivity of 89% and pair.13,14 However, some studies have
Apley grind test, the patient lies 92% and specificity of 97% and reported successful repair of tears
prone with the knee flexed to 90°. 96% for the medial and lateral me- that extend into the avascular zone
The examiner assesses for pain by nisci, respectively.10 of the meniscus, especially in
performing internal and external ro- MRI is typically used to confirm a younger patients.15,16
tation of the leg while applying axial clinical diagnosis. However, its added The length of a tear affects its sta-
load. This test has a sensitivity of value in diagnosis has been disputed; its bility. Tears measuring <1 cm in
41% for both medial and lateral usefulness is largely based on the qual- length are generally considered sta-
tears and a specificity of 93% and ity of the MRI. A prospective study ble, and repair is usually unneces-
86% for medial and lateral meniscal showed accuracy of 73.7% with MRI sary.13,15,17 Tears measuring >4 cm in
tears, respectively. diagnosis and accuracy of 80.7% on length are unstable to the point that
In the McMurray test, the patient clinical examination.11 MRI is not attempted repairs often fail; thus,
lies supine and the knee is flexed to sufficiently accurate to show whether tears of this size are rarely repaired,
90°. Next, the examiner applies a a tear is repairable.12 either.13,14

206 Journal of the American Academy of Orthopaedic Surgeons


Catherine Laible, MD, et al

Figure 4 Figure 5 long enough to develop symptoms


following meniscectomy; however,
persons who undergo meniscectomy
early in life will experience symp-
toms and will suffer a longer dura-
tion of associated morbidities.15
Anterior cruciate ligament (ACL)
tear is the most common injury that
occurs concurrently with meniscal
tear. Outcome studies have demon-
strated that repairs of the meniscus
performed concurrently with ACL
reconstruction are as successful as20
Arthroscopic image of a meniscus or significantly more successful
Arthroscopic image of a meniscus tear that is a poor candidate for
tear that is a good candidate for repair because it is degenerative than13,14,17 repairs performed in ACL-
repair because it is located in the and is located in the peripheral intact knees. This may be the result
red-white zone, is nondegenerative, avascular zone. Such tears should of the release of blood and other
and is of the bucket-handle type. be managed with arthroscopic
A = femoral condyle, B = tibial healing factors into the joint during
débridement.
plateau, C = white zone portion of the ACL reconstruction. There is
bucket-handle tear, D = red zone some debate with regard to, and
portion of bucket-handle tear
cause those tears allow the meniscus some evidence in support of, staged
to extrude from the knee. Moreover, meniscus repair and ACL reconstruc-
Tear shape is another factor in the study shows that normal contact tion.21 However, it is generally rec-
whether repair is possible. Radial mechanics are restored with tear re- ommended that ACL reconstruction
tears are often located in the avascu- pair, which highlights the importance and meniscal repair be performed
lar zone, and as a result, they are of repairing meniscal root tears to concurrently.
typically managed with partial men- preserve normal knee mechanics. Tears of the lateral meniscus are
iscectomy. More substantial radial Controversy persists regarding generally found following acute ACL
tears that extend the entire width of whether the timing of repair affects rupture, and these tears are likely re-
the meniscus may be an indication success. Tengrootenhuysen et al17 lated to the initial injury. Lateral me-
for repair.18 Horizontal tears often found a significantly higher success niscus tears are usually found inci-
are not repaired, in part because it is rate in tears repaired <6 weeks after dentally and are often stable and
difficult to reduce the edges with su- the injury (P < 0.001). In contrast, nondisplaced. Conversely, tears of
tures in these tears, which are ori- other studies have indicated either an the medial meniscus are often found
ented parallel to the plane of the insignificant difference or no differ- in chronically ACL-deficient knees,
knee joint. Additionally, horizontal ence in healing rates.13-16,20 likely resulting from the increased in-
tears are frequently degenerative Traditionally, it has been presumed stability commonly found in these
tears.13,15 Conversely, longitudinal that the menisci of younger patients joints. Typically, these tears are de-
tears are commonly repaired because have a more effective healing re- generative and complex, and often
they are amenable to suture fixation sponse and, thus, that meniscal re- they are not repairable.22 In a meta-
(Figure 4). pair should be favored in these pa- analysis of 10 studies, Pujol and
Tears that appear to be degenera- tients. Outcome studies evaluating Beaufils23 evaluated the healing rates
tive tend to be associated with repair failure rates have questioned of meniscal tears that were neither
chronic damage to the meniscus; typ- this presumption, with some studies repaired nor débrided at the time of
ically, these tears are débrided14 (Fig- showing significantly better success ACL reconstruction. They found a
ure 5). In a biomechanical study in young patients9,12 and others 4.8% incidence of residual pain or
published in 2008, Allaire et al19 showing no difference based on repeat meniscectomy for lateral me-
demonstrated that medial meniscal age.13,16 Regardless, repair should be niscus tears, compared with 14.8%
posterior root tears have an impact favored in young patients because ar- in medial meniscus tears. However,
on tibiofemoral contact mechanics thritic progression following menis- other than stability of the tear, inclu-
almost identical to the impact of cectomy takes years to develop. El- sion criteria varied considerably
complete medial meniscectomy be- derly patients are unlikely to live among the studies.

April 2013, Vol 21, No 4 207


Meniscal Repair

Figure 6 For medial meniscus repair, the more recent mechanical study by
medial incision is made anterior to Aros et al29 found that with high-
the medial head of the gastrocnemius strength suture material, load to fail-
muscle, thereby exposing the cap- ure is the same regardless of suture
sule. For lateral incisions, the dissec- orientation.
tion is made anterior to the lateral All-inside repair devices were de-
head of the gastrocnemius. Care is veloped to reduce surgical time, pre-
taken to avoid neurovascular struc- vent complications resulting from ex-
tures. A sterile spoon or a speculum ternal approaches, and allow access
may be used to retrieve sutures and to tears of the posterior horn. First-
visualize the capsule. Sutures must be generation all-inside techniques in-
tied with the knee in relative exten- volved the insertion of rigid arrow or
sion to prevent capture of the poste- screw implant devices made of ab-
rior capsule of the knee as it folds on sorbable polymers. However, it
Arthroscopic image of a meniscal flexion, thus limiting extension. quickly became apparent that the de-
repair performed with the inside-out The inside-out technique is still vices were prone to breaking30 and to
suturing technique with horizontal
mattress sutures in a left knee. commonly used, although it is very damaging articular cartilage;31 they
difficult technically to repair tears in were abandoned for second-generation
the posterior horns of the menisci headless screws and arrows, which
with this technique.24 Although it has protruded less. These improved rigid
Repair Techniques proved to be effective, this technique fixation devices are still used, although
has a significant learning curve and recent studies have shown them to have
Initially, repairs of meniscal tears typically requires the presence of a less mechanical strength than suture
were approached from the periphery surgical assistant. repairs.32 Järvelä et al33 recently
of the meniscus without arthroscopic In the outside-in technique, sutures showed that of 42 meniscal repairs
instrumentation; thus, only the most are passed through the meniscus performed using meniscal screws and
peripheral tears could be accessed. from the outside, thus avoiding the arrows, 11 failed clinically on
The inside-out suturing technique more extensive incisions and retrac- follow-up, and some exhibited artic-
was the first one used for arthro- tions involved in inside-out repairs. ular cartilage damage.
scopic repair of meniscal tears, and it As with inside-out repairs, however, The third-generation all-inside re-
is still considered to be the standard outside-in repairs are largely limited pair devices involve the insertion of
of care for meniscal repair. to anterior portions of the medial sutures and suture fixators. These
In general, meniscal repair begins and lateral menisci.25 devices have been shown to be clini-
with a complete arthroscopic assess- Prospective studies have indicated cally effective. Grant et al26 found a
ment of the knee and full evaluation success with both techniques. In a pooled failure rate of 14.6% among
of the tear. In patients who require meta-analysis of isolated meniscus three studies in their meta-analysis.
repair, the margins of the tear are dé- repairs, Grant et al26 found a com- A bovine mechanical study showed
brided, with or without rasping. At bined 17% incidence of repair failure third-generation all-inside devices to
that point, the surgeon must decide with the inside-out technique and an have the same or slightly less load to
on a repair technique: inside-out, average Lysholm score of 87.8 on failure than horizontal or vertical
outside-in, all-inside, or a combina- follow-up. In a follow-up study of 41 mattress sutures.29 Third-generation
tion of these. patients with menisci repaired using all-inside suturing systems remain a
With the inside-out technique, su- the outside-in technique, Abdelkafy viable option for meniscal repair.
tures are inserted into the meniscus et al27 found that 5 patients (12%) Fourth-generation repair devices
using a needle cannula under arthro- required subsequent partial menis- allow placement of sutures in the
scopic visualization (Figure 6). The cectomy, and 36 patients had a mean meniscus without the aid of an exter-
needles with suture attached are Lysholm score of 87.3 at a mean of nal incision or a suture fixator sys-
passed on either side of the tear 11.7 years. tem. These new devices are self-
through the meniscus, then out the Mechanical studies have histori- adjusting, with the anchor located
knee through the capsule. An inci- cally shown that vertical mattress su- behind the capsule and with a sliding
sion is made in the skin, and the su- tures provide stronger fixation than knot that can be tensioned appropri-
tures are tied down to the capsule. do horizontal sutures.28 However, a ately by the surgeon. In a mechanical

208 Journal of the American Academy of Orthopaedic Surgeons


Catherine Laible, MD, et al

Figure 7 meniscus tears. Hematoma, aneu-


rysm, and pseudoaneurysm of the
popliteal artery have been described
in the literature. Symptoms often
present within the first 2 to 3 weeks
postoperatively, but can rarely pre-
sent later, up to 10 weeks postopera-
tively.36 In a cadaver study, Cohen
et al37 found that the needles used in
third-generation all-inside repairs of
the posterior horn of the lateral me-
niscus come within a few millimeters
of the popliteal artery (Figure 8).
Some manufacturers include penetra-
tion limiters to minimize vascular
risk, but even with these, surgeons
Illustration of meniscal root tear repair using the tibial tunnel technique. A must take care when performing pos-
2.4-mm tunnel was drilled from the anterolateral aspect of the tibia to the terior repairs.
root insertion site, using an anterior cruciate ligament tunnel guide, and a Complications involving the com-
horizontal mattress suture was passed through the meniscal root. Using a
suture passer, the free ends of the suture were passed through the tunnel, mon peroneal nerve have been re-
then tied over a button under manual tension. (Adapted with permission from ported in lateral meniscus repair. Ju-
Allaire R, Muriuki M, Gilbertson L, Harner CD: Biomechanical consequences rist et al38 published a case report in
of a tear of the posterior root of the medial meniscus: Similar to total
which complete motor neuropathy
meniscectomy. J Bone Joint Surg Am 2008;90[9]:1922-1931.)
was caused by sutures placed in an
inside-out repair. The lateral genicu-
study, Gunes et al34 found that these three most recent generations of all- late artery is also at risk during
repair devices created fixations that inside meniscal repair are all effective inside-out lateral meniscal repair.
were as strong as outside-in sutures options for tear fixation and that Lateral geniculate pseudoaneurysm
and significantly stronger than other they can be used with equal clinical has been reported, and the proximity
all-inside fixation devices. effectiveness. However, the surgeon of this vessel has been well demon-
Meniscal root tears are repaired must be mindful of the risk of device strated in simulated meniscal repairs
differently from other meniscal tears breakage with first- and second- in the laboratory.39
because the meniscal root must be generation all-inside repairs and the The proximity of the saphenous
reaffixed to bone to prevent meniscal risk of neurovascular complications nerve to the medial meniscus can
extrusion. The torn meniscal root is with inside-out and outside-in suture also lead to complications ranging
fixed to the tibial plateau either us- techniques. from transient paresthesia40 to com-
ing sutures attached to suture an- plete neuropathy. Because of varia-
chors in the bone or using an in- tions in anatomy, neurovascular
traosseous suturing technique, then Complications complications can occur separate
passing the meniscal sutures through from the location of the repair.
a tunnel drilled with an ACL tibial Meniscus repair is a relatively fast First- and second-generation all-
tunnel drilling guide and anchoring and noninvasive procedure, and inside rigid meniscal repair devices
them at the anteromedial tibia (Fig- complications are rare. However, are also associated with specific com-
ure 7). Both techniques have been given the proximity of the menisci to plications. These devices can break,
shown to be clinically effective. neurovascular structures, the sur- forming loose fragments that can
However, in some cases, the repair geon must be aware of the risk of damage articular cartilage and cause
does not completely heal, leading to damaging those structures during aseptic reactive synovitis. A case re-
some persistent meniscal extrusion surgery. port has been published of a broken
and subsequent articular cartilage The popliteal artery closely borders device exiting the joint capsule, ne-
degeneration.35 the posterior knee and injury to it is, cessitating surgical removal.30 Al-
Review of the literature suggests perhaps, the most dreaded complica- though the design of rigid implants
that inside-out, outside-in, and the tion in the repair of posterior horn has improved in third- and fourth-

April 2013, Vol 21, No 4 209


Meniscal Repair

Figure 8 Figure 9

Arthroscopic image demonstrating


use of a rasp to access the
Lateral (A) and AP (B) fluoroscopic views demonstrating an all-inside meniscus-synovial junction in
meniscal repair device shown in close proximity to the popliteal artery as preparation for repair of a tear and
demonstrated on angiography. No depth penetration limiter was used in this to introduce hematogenous healing
case. (Reproduced with permission from Cohen SB, Boyd L, Miller MD: factors into the joint space.
Vascular risk associated with meniscal repair using Rapidloc versus Fas
T-Fix: Comparison of two all-inside meniscal devices. J Knee Surg
2007;20[3]:235-240.) ogous blood that has been spun in a
centrifuge until the concentration of
platelets is above baseline levels. The
generation devices, even headless published a retrospective study that
two PRP injection systems that are
screws and arrows may become ex- demonstrated complete healing in
currently approved by the US Food
posed and cause damage to the sur- 71% of treated menisci following
and Drug Administration yield plate-
rounding cartilage.31 meniscal rasping at second-look ar- let concentrations four to five times
throscopy. However, 44 of 48 tears greater than normal. PRP is theo-
were associated with an ACL tear. rized to have a beneficial effect on
Repair Enhancement
Trephination is a controversial tech- healing because of the high levels of
Multiple augmentation techniques nique that involves the creation of growth factors, including platelet-
are available to optimize the healing vascular channels to connect the derived growth factor, transforming
potential of meniscal repair. Periph- avascular meniscus to the peripheral growth factor β, fibroblast growth
eral tears are known to have a closer perimeniscal blood supply. A spinal factor, insulin-like growth factors
proximity to the perimeniscal blood needle is used to puncture the menis- (IGFs [ie, IGF-1, IGF-2]), vascular
supply and, therefore, to heal more cus through the area of the repair; endothelial growth factor, and
predictably. Most augmentation the needle is directed toward the pe- interleukin-8. Combining the PRP
techniques are performed with the riphery. In a goat model, such chan- with an activating agent, such as
intent to enhance the healing of more nels were shown to result in the stim- thrombin or calcium chloride, results
central meniscal tears. ulation of fibrochondrocytes, leading in the release of growth factors.
Fibrin clots are created by spinning to a reparative process involving fi- When injected near or sutured into a
autologous blood in a glass tube un- brovascular tissue.44 However, it has meniscal repair, the proximity of
til a clot is formed. Henning et al41 been suggested that these channels these growth factors may stimulate
showed that incorporation of a fibrin can disrupt the circumferential colla- collagen synthesis and promote an-
clot into an isolated meniscal repair gen fibers of the meniscus. giogenesis and neovascularization.
resulted in a failure rate of 8%, com- Other techniques to enhance me- No randomized, controlled trials in-
pared with 41% without the clot. niscal repairs are being studied and vestigating the use of PRP in menis-
Meniscal abrasion using a meniscal are being used by some surgeons. cal repairs are underway.
rasp (Figure 9) or arthroscopic shaver However, there is currently no medi- Newer biologic enhancement tech-
has been shown to promote the heal- cal literature that formally evaluates niques have been discussed recently.
ing response through the expression of them. Hyaluronic acid injections following
cytokines.42 In 2003, Uchio et al43 Platelet-rich plasma (PRP) is autol- meniscal repair have been shown in

210 Journal of the American Academy of Orthopaedic Surgeons


Catherine Laible, MD, et al

animal models to result in faster pair location and type.46 During this the importance of adhering to the re-
healing and better defect fill.45 Cell- period, the patient also must refrain habilitation protocol postoperatively.
based therapy involving the growth from participating in sports that in-
of autologous chondrocytes on an volve running or cutting.
implanted scaffold as well as the in- Some studies have shown that an References
jection of specific growth factors to accelerated rehabilitation program,
stimulate meniscal cells and augment including unrestricted weight bearing Evidence-based Medicine: Levels of
meniscal repair are being tested in and a return to sports activity as evidence are described in the table of
animal studies. No formal studies soon as it is tolerated, is no less ef- contents. In this article, reference 33
have been published to date regard- fective than standard, more conser- is a level I study. Reference 35 is a
ing outcomes of these techniques. vative, meniscal repair rehabilitation level II study. References 11, 14, 18,
programs in preventing repair fail- 28, 29, 37, 40, 43, and 48 are level
ures.50 However, currently, there is III studies. References 4, 10, 12, 15-
Rehabilitation insufficient corroborated evidence to 17, 20-27, 32, 34, 42, 44, 47, and 49
support the use of accelerated reha- are level IV studies. References 1-3,
The postoperative limitations of me- bilitation following meniscal repair. 5-9, 13, 30, 31, 36, 38, 39, 41, 45,
niscal repair are markedly greater 46, and 50 are level V expert opin-
than those of partial meniscectomy. ion.
Because it is impossible to know for Summary References printed in bold type are
certain before surgery whether a me- those published within the past 5
niscal tear is repairable, it is impor- Arthroscopic management of menis- years.
tant that patients be well-informed cal injury is the most commonly per-
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surgeon may choose to allow the pa- meniscus repair has increased. 2. Athanasiou KA, Sanchez-Adams J:
Structure-function relationships of the
tient to bear weight with the knee Factors shown to be predictive of a
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the menisci is significantly increased egory but are deemed appropriate 90-95.
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those actions can put undue stress on the standard of care for meniscus re- the meniscus. Operative Techniques in
the repair in the early stages of heal- Sports Medicine 2003;11(2):68-76.
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measurement of static pressure
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tion and type of repair performed.46 Eng 1983;105(3):216-225.
for tear fixation. Knowledge of the
Because of the increased strain on surrounding neurovascular struc- 7. Makris EA, Hadidi P, Athanasiou KA:
The knee meniscus: Structure-function,
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deep flexion, deep squats and exces- sociated with each specific meniscal techniques, and prospects for
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least 4 months postoperatively.48,49 tion protocol is required, and the pa- Dynamic contact mechanics of the
The duration varies depending on re- tient must understand preoperatively medial meniscus as a function of radial

April 2013, Vol 21, No 4 211


Meniscal Repair

tear, repair, and partial meniscectomy. Arthroscopic repair of meniscus tears meniscal repairs: An in vitro
J Bone Joint Surg Am 2010;92(6):1398- extending into the avascular zone with biomechanical evaluation. Am J Sports
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Catherine Laible, MD, et al

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April 2013, Vol 21, No 4 213


Review Article

Snapping Scapula Syndrome:


Diagnosis and Management

Abstract
Trevor Gaskill, MD Scapulothoracic bursitis and snapping scapula syndrome are rare
Peter J. Millett, MD, MSc diagnoses that contribute to considerable morbidity in some
patients. These conditions represent a spectrum of disorders
characterized by pain with or without mechanical crepitus. They are
commonly identified in young, active patients who perform
repetitive overhead activities. Causes include anatomic scapular or
thoracic variations, muscle abnormalities, and bony or soft-tissue
masses. Three-dimensional CT and MRI aid in detecting these
abnormalities. Nonsurgical therapy is the initial treatment of choice
but is less successful than surgical management in patients with
anatomic abnormalities. In many cases, scapular stabilization,
postural exercises, or injections eliminate symptoms. When
nonsurgical treatment fails, open and endoscopic techniques have
From the Naval Medical Center
been used with satisfactory results. Familiarity with the
Portsmouth, Portsmouth, VA
(Dr. Gaskill), and The Steadman neuroanatomic structures surrounding the scapula is critical to
Clinic, Vail, CO (Dr. Millett). avoid iatrogenic complications. Although reported outcomes of both
Dr. Millett or an immediate family open and endoscopic scapulothoracic decompression are
member has received royalties from
Arthrex; serves as a paid consultant
encouraging, satisfactory outcomes have not been universally
to Arthrex; has stock or stock achieved.
options held in Game Ready and
VuMedi; and has received research
or institutional support from Arthrex,
OrthoRehab, Össur Americas,
Siemens USA, Smith & Nephew,
and ConMed Linvatec. Neither
S capulothoracic articulation is
unique in that the concave scap-
ula must glide smoothly on the con-
drome has improved, and surgical
management has evolved. Patient-
reported outcome measures and return
Dr. Gaskill nor any immediate family
member has received anything of vex thoracic cage to provide a func- to sport have been integrated into out-
value from or has stock or stock tional foundation for glenohumeral come studies; assessment of results
options held in a commercial
motion. Although several bursal and based on these stringent criteria suggest
company or institution related
directly or indirectly to the subject of soft-tissue planes facilitate this mo- that although significant improvement
this article. tion, it remains an innately irregular of symptoms can be achieved with sur-
The views expressed in this article articulation. Despite this irregularity, gery, complete resolution is not univer-
are those of the author(s) and do bursitis and snapping scapula syn- sal. Therefore, despite recent advances,
not necessarily reflect the official drome remain relatively rare diagno- diagnosis and management of snapping
policy or position of the Department
ses. Symptoms vary from intermit- scapula syndrome remains challenging.
of the Navy, the Department of
Defense, or the US Government. tent, mildly symptomatic bursitis to
debilitating, recalcitrant crepitus.
J Am Acad Orthop Surg 2013;21: Anatomy and Physiology
214-224 Early recognition and management
are essential to minimize unnecessary
http://dx.doi.org/10.5435/ Bony Structure
JAAOS-21-04-214
disability.
Since its initial description in 1867 Scapulothoracic articulation is
Copyright 2013 by the American
by Boinet,1 understanding of the path- unique in that it does not exhibit a
Academy of Orthopaedic Surgeons.
omechanics of snapping scapula syn- true synovial articulation. Scapular

214 Journal of the American Academy of Orthopaedic Surgeons


Trevor Gaskill, MD, and Peter J. Millett, MD, MSc

Figure 1 trast, the serratus anterior muscle


originates from the ribs and inserts
along the medial scapular border.
The long thoracic nerve innervates
the muscle anteriorly, and the nerve
is generally at low risk of injury dur-
ing an open or arthroscopic surgical
approach.
The levator scapulae and rhom-
boid musculature originate from the
midline and insert along the medial
border of the scapula. The dorsal
scapular nerve and artery run deep
to these muscles approximately 1 to
2 cm medial to the scapula. These
neurovascular structures are at risk
of injury during an open approach or
with aberrant arthroscopic portal
placement.

Scapulothoracic Bursae
Both anatomic and adventitial bur-
Illustration of right posterior shoulder demonstrating anatomic and adventitial
bursae of the scapulothoracic joint. sae within the scapulothoracic artic-
ulation have been described3 (Figure
1). Anatomic bursae are thought to
be physiologic; they facilitate gliding
of surfaces within the scapulotho-
motion and stability are controlled Muscular Anatomy racic joint (Figure 2). In anatomic
dynamically through muscular con- studies, two bursae have been consis-
Normal scapulothoracic motion is
traction. The scapula itself lies be- tently found: the infraserratus bursa
the result of several muscles working
tween the second and seventh ribs and the supraserratus bursa, which
in concert to orient the scapula be-
and is characterized by three borders are separated by the serratus anterior
cause no direct bony articulation ex-
(medial, lateral, and superior) and muscle.3 The infraserratus bursa fa-
ists. Dysfunction of any of these
three angles (inferomedial, supero- cilitates gliding of the serratus ante-
muscles may result in abnormal
medial, and lateral). The costal sur- rior muscle on the chest wall, while
scapulothoracic motion. The trape- the supraserratus bursae divides the
face of the scapula undulates, and
thickness ranges from 10.5 to 26.7 zius has a midline origin and inserts serratus anterior and subscapularis
mm.2 The superior and inferior scap- along the superior lip of the scapular muscles.4
ular angles exhibit considerable vari- spine, superficial to the rhomboid Adventitial bursae are typically
ability; the angle of junction with the musculature. It is innervated by the considered pathologic and are com-
scapular body ranges from 124° to spinal accessory nerve, which runs monly present near the superior or
162°.2 The ventral surface of the deep to the muscle with the trans- inferior scapular angles. Identifica-
scapula is concave and articulates on verse cervical artery. The concave tion of these bursae is inconsistent in
the convex chest wall. The supra- scapula glides along the convex chest anatomic studies, and their presence
scapular notch lies along the medial wall, using the serratus anterior and is thought to represent a pathologic
aspect of the lateral third of the su- subscapularis muscles as a soft-tissue state.5,6 Symptoms occurring along
perior border of the scapula. The articulation. The subscapularis origi- the inferior scapular angle are typi-
transverse scapular ligament sepa- nates from the anterior surface of the cally secondary to bursal tissue lying
rates the suprascapular nerve within scapula and is innervated along its between the serratus anterior and the
the notch from the suprascapular ar- anterior border by the upper and chest wall.7,8 Debate exists, however,
tery coursing above it. lower subscapular nerves. In con- regarding the anatomic location of

April 2013, Vol 21, No 4 215


Snapping Scapula Syndrome: Diagnosis and Management

Figure 2 bursal tissue when the superior angle


of the scapula is symptomatic. Stud-
ies have reported bursal tissue lo-
cated between the serratus anterior
muscle and chest wall (ie, infraserra-
tus bursa)9 or between the subscapu-
laris and serratus anterior muscles
(ie, supraserratus bursa).10 Occasion-
ally, patients experience pain along
the medial base of the scapular spine
caused by a trapezoid bursa located
deep to the trapezius muscle near the
medial attachment of the scapular
spine.

Neurovascular Anatomy
Several neurovascular structures
course within the scapulothoracic
articulation to innervate the sur-
rounding musculature (Figure 3). A
Illustration of an axial cross-section of the scapulothoracic articulation. Note thorough understanding of the neu-
the location of bursae in relation to muscular planes. roanatomy of this region is critical to
minimize the risk of iatrogenic com-
plications. Ultimately, the risk to in-
dividual neurovascular structures is
Figure 3 dependent upon the surgical ap-
proach used for bursal decompres-
sion. The spinal accessory nerve is
located along the middle section of
the levator scapulae muscle deep to
the trapezius muscle.11 The main
branches of the spinal accessory
nerve are at risk of injury with portal
placement cranial to the scapular
spine or with inadvertent dissection
during open approaches. Typically,
the dorsal scapular nerve is identified
deep to the rhomboid major and mi-
nor muscles, 1 to 2 cm medial to the
medial border of the scapula.11 The
transverse scapular artery gives rise
to deep and superficial branches,
with the deep branch forming the
dorsal scapular artery and accompa-
nying the dorsal scapular nerve. The
superficial branch runs along the spi-
nal accessory nerve. These structures
Illustration of the right posterior shoulder demonstrating the gross location of are at risk of injury with medial
neurovascular structures important in scapulothoracic articulation. Black dots placement of arthroscopic portals or
indicate typical portal locations, with the distance from medial scapular
border noted. medial dissection during an open sur-
gical approach.

216 Journal of the American Academy of Orthopaedic Surgeons


Trevor Gaskill, MD, and Peter J. Millett, MD, MSc

The long thoracic nerve innervates namic disorders that are the result of ondary to either scapular or thoracic
the serratus anterior muscle and runs predisposing abnormal anatomy cage anatomic variation.
along the anterior belly of the mus- combined with sufficient scapulotho-
cle. Unless dissection is performed racic motion. Symptoms may be ex- Scapulothoracic Masses
considerably more lateral than is typ- perienced with minimal activity if
Several scapulothoracic masses can
ical, this nerve is infrequently at risk considerable bony abnormality is
also result in crepitation. Osteochon-
of injury during arthroscopic or open present. Alternatively, repetitive
droma of the rib or scapula is the
surgical techniques. After branching overuse may incite symptoms even in
most frequently reported mass re-
from the brachial plexus, the supra- the presence of normal anatomy and
sponsible for scapulothoracic symp-
scapular nerve and artery pass to- may result in a spectrum of severity
toms, and resection is frequently cu-
ward the suprascapular notch before ranging from mild soreness to debili-
innervating the rotator cuff muscula- tating crepitus. rative18,19 (Figure 4). Infrequently,
ture. The suprascapular nerve and Scapulothoracic bursitis is thought scapular chondrosarcoma may be en-
artery are at risk of injury if a su- to be the result of inflammation countered in older patients, thereby
peromedial scapular resection is per- caused by overuse of the shoulder emphasizing the need for diligent di-
formed or a superior arthroscopic girdle. If sufficient irritation is pres- agnostic evaluation. The presence of
portal is used. Placement of the por- ent to create a chronic inflammatory an elastofibroma dorsi in the in-
tal at the junction of the medial two environment, fibrosis of the affected frascapular region is also occasion-
thirds and lateral third of the supe- bursa may occur. Fibrosis may ulti- ally reported. In this location, the
rior scapular border generally pro- mately lead to recalcitrant bursitis or mass is capable of elevating the infe-
vides ≥10 mm of distance from the snapping even in the absence of overt rior scapular border, thereby creating
suprascapular nerve.12 The use of scapular masses or muscular abnor- mechanical symptoms.20
bony landmarks for superomedial malities.6,10
border resection generally aids the Overt scapular snapping is fre- Scapular Angulation
surgeon in maintaining a 2-to 3-cm quently the result of bony or soft- The angle of the superomedial scapula
margin from the suprascapular tissue masses within the scapulotho- may also predispose some patients to
notch.12,13 racic articulation and may coexist scapulothoracic dysfunction. The su-
with scapulothoracic bursitis. A peromedial scapula and scapular body
spectrum of mechanical causes re- normally form an angle that measures
Pathophysiology sults in crepitus, including fibrotic or between 124° and 162°, and anatomic
anomalous musculature7,14,15 and abnormalities in this area may result in
Under physiologic conditions, the malunion of scapular or rib frac- incongruity, focal loading, inflamma-
concave anterior scapula glides tures.16 Variability in the anatomy of tion and, if the angle is of sufficient
smoothly over the convex thoracic the costal or scapular surfaces is magnitude, crepitus.2 Cadaver stud-
cage during shoulder motion. This common and may also influence ies suggest that approximately 6% of
motion is critical to provide a stable scapulothoracic snapping.2 This is scapulae may demonstrate some de-
foundation for glenohumeral func- exemplified by scapulothoracic crep- gree of superomedial hooking, and
tion. The scapulothoracic articula- itus associated with scoliosis and ky- 8.6% of scapular specimens exhibit
tion is unique in that it glides upon phosis17 and the resolution of symp- superomedial angulation ≥35°.21
muscular layers rather than cartilagi- toms with postural training in some Similar bony abnormality is occa-
nous surfaces, and it has been de- patients.10 In addition, resection of sionally identified along the inferior
scribed as perhaps the most incon- the first rib for management of tho- scapular angle, which appears to be
gruent articulation in the human racic outlet syndrome may elicit the second most common site of
body. To this end, the presence of snapping of the scapula.15 In a study symptoms.21 Osteochondroma or a
bursal tissue is physiologic and nec- of 13 patients with thoracic outlet Luschka tubercle (ie, a bony protu-
essary to facilitate normal scapu- syndrome who underwent first-rib berance of the superomedial scapular
lothoracic motion. However, as in resection and later developed snap- border) can also result in persistent
other musculoskeletal disorders, ab- ping scapula syndrome, scapula symptoms.7 It is important to note,
normal stress persistently applied to symptoms resolved in 9 patients however, that scapular crepitus may
normal structures can result in dys- (70%) after resection of the supero- be present in asymptomatic patients.
function. Thus, scapulothoracic syn- medial scapular border. Therefore, Therefore, mechanical symptoms
dromes can be thought of as dy- scapular crepitation may occur sec- alone should not be considered

April 2013, Vol 21, No 4 217


Snapping Scapula Syndrome: Diagnosis and Management

Figure 4 ances may contribute to a pathologic


state. The trapezius, rhomboid, leva-
tor scapulae, serratus anterior, and
lattisimus dorsi muscles should be
tested specifically. The rhomboids
and levator scapulae muscles are best
tested by placing the hands along the
iliac crest and pressing the scapulae
together by moving the elbows in a
posterior direction. Dysfunction of
the serratus anterior can be identified
clinically by noting the presence of
medial scapular winging while the
patient performs a wall pushup. Oc-
casionally, patients are able to dem-
onstrate activities or specific motions
Plain AP radiograph (A) and axial CT scan (B) of the left shoulder that result in scapulothoracic crepi-
demonstrating a scapulothoracic osteochondroma that can be seen along the tus. Careful observation and palpa-
medial border of the scapula (asterisk) and within the scapulothoracic
articulation (arrow). tion while the patient is re-creating
the crepitus often aids in localizing
the pathologic scapular segment.
Motions that result in scapulotho-
pathologic unless they are associated racic crepitus may be accentuated if
Physical Examination
with pain or functional loss. the scapula and thoracic cage are
A thorough physical examination is compressed during shoulder abduc-
critical to identify an anatomic etiol- tion.14
Clinical Presentation ogy for the patient’s symptoms. The
examination should begin with an Imaging
History inspection of the cervical and tho-
Plain radiographs should be ob-
racic spine for fixed or postural ky-
Patients who present with scapu- tained to screen for osseous abnor-
phosis that may contribute to scapu- malities that may contribute to scap-
lothoracic bursitis or snapping often
have experienced symptoms for a lothoracic incongruity.5 Cervical ular bursitis or crepitus. Routine
considerable period of time. Present- degeneration may be responsible for radiography includes AP, lateral, and
ing complaints encompass a spec- referred pain syndromes. Extremity axillary views in the plane of the
trum of symptoms ranging from range of motion should be tested, scapula. When a lesion is identified
mild, intermittent discomfort to no- with specific attention paid to scapu- or suspected, the threshold for ob-
table functional disability. Some pa- lothoracic motion. Active and pas- taining three-dimensional imaging is
tients may report decreased athletic sive scapulothoracic and glenohu- low. CT scans provide excellent bony
performance, but many experience meral motion is evaluated for detail, improving identification and
increased pain with overhead activi- resultant crepitus. Dynamic exami- characterization of bone masses.
ties. Patients may also report audible nation of the scapula may demon- Mozes et al24 compared the use of
or palpable crepitus, which encom- strate scapular winging resulting plain radiography, CT, and three-
passes a spectrum of severity. It is from motor dysfunction or scapu- dimensional CT for evaluation of
important to note that bursitis and lothoracic masses. Pseudowinging snapping scapula syndrome in 20 pa-
scapular snapping may exist inde- may also be present if the patient is tients (26 scapulae). The authors re-
pendently or concomitantly. Trau- compensating for pain or has learned ported that scapulothoracic incon-
matic etiology22,23 and overuse syn- motion patterns to avoid crepitus.10 gruity was identified on plain
drome8,23 are both commonly Tenderness and bursal fullness may radiographs in 7 of 26 scapulae,
reported. Cobey5 suggested a familial be identified in the symptomatic whereas incongruity was identified
propensity for crepitus at the supe- scapular region. Muscular strength on CT and three-dimensional CT
rior border of the scapula. should be evaluated because imbal- scans in 19 of 26 and 26 of 26 scap-

218 Journal of the American Academy of Orthopaedic Surgeons


Trevor Gaskill, MD, and Peter J. Millett, MD, MSc

Figure 5 injection may be therapeutic.6 Ultra- combination of shoulder girdle


sound guidance can be helpful for in- strengthening, diathermy, ultra-
jection localization, and care should sound, and iontophoresis. Similarly,
be taken to avoid thoracic perfora- Groh et al33 reported good or excel-
tion or intravascular injection. Hod- lent results in 22 of 30 patients
ler et al27 reported that 18 of 20 pa- treated with periscapular strengthen-
tients with subscapular pain treated ing. Therefore, symptomatic im-
with fluoroscopy-guided scapulotho- provement can be achieved with ap-
racic injection experienced symptom- propriate nonsurgical measures, but
atic relief. Others have reported simi- diligence is required, and nonsurgical
lar results following scapulothoracic
management appears to be most suc-
injection.28-30 Symptomatic improve-
cessful in patients with no scapu-
ment following the injection can help
lothoracic masses.7
substantiate the diagnosis and con-
firm the anatomic location of the
Three-dimensional CT scan of the
symptomatic bursa.
Surgical
posterior right scapula. Note the
superomedial scapular border Indications
resection (asterisk). Surgical intervention is considered in
Management the setting of scapulothoracic bursi-
tis or snapping scapula syndrome
ulae, respectively. On the basis of Nonsurgical when nonsurgical treatment has
these findings, three-dimensional CT In the absence of an aggressive lesion, failed to yield symptomatic improve-
may best delineate potential bony ir- a trial of nonsurgical management is ment. Outcomes of surgical interven-
regularities responsible for scapu- warranted. Initial phases of rehabilita- tion may be more reliable if the pa-
lothoracic irritation (Figure 5). MRI tion focus on minimizing inflammation tient experiences symptomatic relief
is more effective than CT for identifi- through activity modification and non- following local anesthetic injection
cation of inflamed bursae and soft- steroidal anti-inflammatory drugs.31 of the symptomatic bursae.10,17,30
tissue masses. Distended bursae may Steroid injections also can be useful Thus, the lack of symptomatic im-
resemble soft-tissue tumors in some for decreasing symptoms and facili- provement after a diagnostic injec-
circumstances.25 Recent advances in tating rehabilitation. tion should be considered a relative
imaging techniques and field Physical therapy should focus on contraindication to surgical interven-
strength have improved the useful- periscapular muscle strengthening tion.29 Patients who exhibit cervical
ness of MRI to characterize abnor- and postural training exercises.8 An spine disorders, neurologic deficits,
mal anatomy and inflamed scapu- upright posture helps to reduce ky- or periscapular wasting should be
lothoracic bursae; however, bony phosis and may improve scapulotho- carefully evaluated before surgical
resolution remains limited compared racic congruency. Periscapular mus- intervention.29
with that of CT.26 culature retraining should include
low-intensity, high-repetition exer- Open Technique
Diagnostic Injections cises that focus on the subscapularis Surgical intervention for bursitis and
Selective injections of local anes- and serratus anterior muscles.32 Mo- snapping scapula syndrome may be
thetic or a steroid can be useful for dalities such as ice, heat, and ultra- accomplished using an open ap-
identification of symptomatic bur- sound also have been used, with proach with the patient positioned
sae. A 22-gauge needle is placed varying levels of success.6,10 Because prone.14,29 The surgical extremity is
along the scapula in the area of max- these modalities are unlikely to con- commonly draped free. A vertical in-
imal tenderness. The injection can be tribute to additional scapulothoracic cision is made overlying the medial
given with the patient positioned symptoms, they may be applied liber- border of the scapula and centered
prone and the arm internally rotated ally. Physical therapy is frequently over the symptomatic bursa (Figure
maximally, with the hand placed successful in patients with no overt 6). After dissection of subcutaneous
along the small of the back. If the masses; however, 6 months or more tissue, the trapezius muscle is split in
patient experiences transient relief, of therapy may be necessary.17 line with its fibers over the scapular
an inflammatory process is likely Ciullo3 reported excellent outcomes spine. Preservation of the spinal ac-
present.8 In some circumstances, the in 62 of 72 patients treated with a cessory nerve, which crosses just lat-

April 2013, Vol 21, No 4 219


Snapping Scapula Syndrome: Diagnosis and Management

Figure 6

Illustrations demonstrating the technique for open scapular resection and bursectomy. A, An incision is made overlying
the medial scapular border. B, The trapezius is split and retracted, exposing the deep posterior shoulder musculature.
C, Muscles are detached subperiosteally as necessary to adequately expose the scapula for resection (dashed line).
D, After scapular resection, sutures are used to reattach the detached muscles to the scapular border.

eral to the superomedial scapular an- subperiosteally, with care taken to crepitation or recurrent bursitis if in-
gle and deep to the trapezius, is protect the dorsal scapular nerve lo- dicated. Ultimately, the detached
critical.34 To provide adequate scapu- cated 2 cm medially. After bursal ex- musculature is reattached through
lar exposure, the rhomboids and le- cision, the angle of the scapula can scapular drill holes with heavy non-
vator scapulae muscles are elevated be excised to alleviate mechanical absorbable suture. A similar tech-

220 Journal of the American Academy of Orthopaedic Surgeons


Trevor Gaskill, MD, and Peter J. Millett, MD, MSc

Figure 7 Figure 8 along the superior scapular border to


aid orientation and to mark the lat-
eral extent of the arthroscopic scapu-
lar resection.35 A shielded round burr
is used to perform the partial
scapulectomy, removing the convex-
ity of a portion of the scapula if nec-
essary (Figure 9). A dynamic exami-
nation is then performed to ensure
adequate resection, the portals are
closed, and the shoulder is placed in
a standard sling.
Intraoperative photograph
demonstrating patient positioning The suprascapular nerve is at risk
Arthroscopic image of the right
for an arthroscopic approach. The shoulder viewed from the
of injury along the lateral one third
patient is positioned prone with the inferomedial portal after partial of the scapula during bony resection.
arm in the “chicken wing” position. resection of the infraserratus bursa. To avoid injury, surgical instruments
The portals (asterisks) are placed a Note the location of rhomboid and
minimum of 3 cm from the medial should not pass lateral to the spinal
chest wall musculature.
scapular border to minimize the needle placed to mark the resection
risk of injury to neurovascular goal. Creation of a superior (Bell)
structures.
cal hemostasis. Portals are bluntly es- portal located at the junction of the
tablished 3 cm medial to the medial medial one third and lateral two
nique has been successfully used to scapular border and inferior to the thirds of the superior scapular bor-
remove the infraserratus bursae in a scapular spine to avoid the dorsal der can also be helpful to facilitate
small series of professional baseball scapular nerve and vessels.11 The ini- scapular resection.13,38
players.8 tial portal is placed at the level of the
inferior angle of the scapula. The
Arthroscopic Technique trochar should be placed as parallel Management of
As arthroscopic skill has improved, to the chest wall as possible to avoid Scapulothoracic Masses
endoscopic techniques have been in- thoracic penetration.11
troduced to manage snapping scap- A 30° arthroscope is inserted The presence of a scapulothoracic
ula syndrome.35,36 Similar to other ar- through the inferior scapular portal, mass requires an appropriate onco-
throscopic procedures, endoscopic and a diagnostic arthroscopy is per- logic work up to confirm a benign
techniques offer the ability to pre- formed. Under direct visualization, a etiology. If an osteochondroma or
serve muscular attachments to the second arthroscopic portal is made elastofibroma are confirmed, the sur-
scapula, which may decrease the just inferior to the medial confluence gical approach is frequently dictated
need for immobilization and facili- of the scapular spine. Within the in- by the location and size of the mass.
tate accelerated rehabilitation time- fraserratus bursae, the intercostal Pedunculated osteochondromas are
lines.37 It is important to note, how- muscles should be visualized inferi- easily removed arthroscopically,
ever, that an optimal approach has orly, the rhomboid and levator mus- whereas elastofibromas or particu-
not yet been defined in the literature. culature medially, and the subscapu- larly large or sessile osteochondro-
Similar to open approaches, the laris laterally (Figure 8). The bursa is mas may be better managed with an
patient is positioned prone and the then excised, with care taken to open surgical approach.
affected extremity is draped free avoid excision of muscle fibers. We Controversy exists regarding
(Figure 7). The arm is placed in near prefer to skeletonize the superome- whether a partial scapuloplasty
maximal internal rotation by placing dial border of the scapula with a ra- should be performed in the absence
the dorsum of the hand in the small diofrequency ablator regardless of of an identifiable bony mass. In gen-
of the back. Functionally, this posi- whether a partial scapulectomy is to eral, partial scapuloplasty is per-
tion increases the potential space be- be performed. This ensures resection formed only if the scapular angle is
tween the scapula and chest wall, fa- of the symptomatic supraserratus or prominent, as visualized arthroscopi-
cilitating safe portal placement.35,36 infraserratus bursa in this location. If cally or radiographically. In a study
The infraserratus bursa is insufflated necessary, a spinal needle can be of 13 patients with scapular snap-
for distension and to improve surgi- placed under fluoroscopic guidance ping, bone from the superomedial

April 2013, Vol 21, No 4 221


Snapping Scapula Syndrome: Diagnosis and Management

Figure 9 all patients, with improvement in


American Shoulder and Elbow Sur-
geons and visual analog scale pain
scores. McCluskey and Bigliani23 re-
ported similar results in a series of
nine patients with refractory scapu-
lothoracic bursitis treated surgically,
with six excellent and two good out-
comes. One poor outcome secondary
to a spinal accessory nerve injury
also was reported. Finally, Arntz and
Matsen22 reported that 12 of 14
shoulders treated with partial
scapulectomy had complete pain re-
A, Arthroscopic image of the left scapula viewed from the inferomedial portal lief at a 42-month follow-up.
demonstrating the superomedial scapular border. B, Arthroscopic image Approaches that incorporate ar-
demonstrating the completed resection of the superomedial border. Note the
absence of the hooked superomedial border of the scapula; the throscopic bursectomy and mini-
supraspinatus musculature (asterisk) can be visualized, as well. open scapulectomy have also been
described for management of snap-
ping scapula syndrome. Lien et al40
performed this technique in 12 pa-
angle was resected if it was promi- atively to facilitate muscular healing.
tients; at a mean 3-year follow-up,
nent during arthroscopy.28 At final The patient can begin pendulum and
the authors reported that American
follow-up, 9 patients reported im- passive motion exercises shortly after
Shoulder and Elbow Surgeon scores
provement of symptoms. Others surgery. Active motion is typically
improved from 36.3 preoperatively
have reported poorer outcomes at a initiated at approximately 8 weeks,
to 88.3 postoperatively. Visual ana-
minimum 2-year follow-up in pa- depending on the type of muscular
log scale pain scores also decreased
tients who did not undergo partial repairs performed. Strengthening ex-
from 8.3 preoperatively to 2.3 post-
scapulectomy compared with those ercises are begun at approximately
operatively. The authors concluded
who received a partial scapulec- 12 weeks, followed by a progressive
that the combined technique was a
tomy.32,39 Therefore, some authors functional regimen that focuses on
reliable alternative treatment option
suggest that excision of the symp- strengthening of periscapular muscu-
for snapping scapula syndrome.40
tomatic scapular angle be performed lature. In contrast, after arthroscopic
Moreover, Lehtinen et al29 found no
in all settings. Although prospective decompression, a sling is used for
statistical difference between open
studies that directly compare out- comfort and is discontinued within
and arthroscopic techniques with re-
comes of patients treated with or the first postoperative week. Passive
gard to successful outcome; however,
without partial scapulectomy are motion and pendulum exercises are
this study was likely underpowered.
lacking, some evidence suggests that begun immediately. Progression to
Arthroscopic techniques represent
scapuloplasty may have a positive in- active motion and strengthening oc-
the most recent evolution in surgical
fluence on patient outcomes regard- curs based on patient tolerance.
management of snapping scapula
less of the presence of mechanical
syndrome. Arthroscopic techniques
symptoms.39
Outcomes may facilitate early functional recov-
ery, decrease hospital stay, and pro-
Rehabilitation The literature suggests that both vide a cosmetic advantage compared
open and arthroscopic management with alternative techniques.18 Several
Although rehabilitation protocols of snapping scapula syndrome can authors have reported that outcomes
vary, timing of rehabilitation de- provide symptomatic improvement. of arthroscopic surgery are similar to
pends on the surgical approach used In a prospective study of 17 patients those of open and combined ap-
for bursal and scapular decompres- with snapping scapula syndrome proaches.3,18,28,41 Recently, Millett
sion. If an open technique is used, treated with open scapulothoracic et al39 reported on a series of 21 pa-
the shoulder is typically immobilized bursectomy, Nicholson and Duck- tients with snapping scapula syn-
in a sling for up to 4 weeks postoper- worth30 reported good outcomes in drome who underwent arthroscopic

222 Journal of the American Academy of Orthopaedic Surgeons


Trevor Gaskill, MD, and Peter J. Millett, MD, MSc

scapulothoracic bursectomy. Signifi- cessful in providing adequate relief 10. Kuhn JE, Plancher KD, Hawkins RJ:
Symptomatic scapulothoracic crepitus
cant improvement of symptoms was of symptoms. Regardless of the sur- and bursitis. J Am Acad Orthop Surg
noted at a minimum 2-year follow- gical approach used, familiarity with 1998;6(5):267-273.
up. Moreover, the authors noted that the neuroanatomic structures that 11. Ruland LJ III, Ruland CM, Matthews
those patients who underwent bur- surround the scapula is critical to LS: Scapulothoracic anatomy for the
sectomy and partial scapulectomy arthroscopist. Arthroscopy 1995;11(1):
avoid iatrogenic complications. Al-
52-56.
experienced better outcomes than though reported outcomes of open
did those who underwent bursec- 12. Aggarwal A, Wahee P, Aggarwal AK,
and endoscopic scapulothoracic de- Kaur H, Sahni D: Anatomical
tomy alone.39 Pearse et al28 reported compression are encouraging, satis- considerations for safe scapular resection
similar results in a study of 13 pa- factory outcomes are not universally in snapping scapula syndrome. Surg
tients; 9 patients reported improve- Radiol Anat 2012;34(1):43-47.
achieved.
ment in symptoms following bursec- 13. Bell SN, van Riet RP: Safe zone for
tomy with or without partial arthroscopic resection of the
superomedial scapular border in the
scapulectomy. Thus, arthroscopic References treatment of snapping scapula syndrome.
management appears to be a reliable J Shoulder Elbow Surg 2008;17(4):647-
649.
management method for snapping Evidence-based Medicine: Levels of
scapula syndrome. 14. Milch H: Partial scapulectomy for
evidence are described in the table of snapping of the scapula. J Bone Joint
Surgical results are now commonly contents. In this article, references 1, Surg Am 1950;32(3):561-566.
measured based on patient-specific 3, 5-8, 14-16, 18-20, 22-30, 32, and 15. Wood VE, Verska JM: The snapping
outcome measures and the ability to 39-41 are level IV studies. Reference scapula in association with the thoracic
return to the prior level of sport, in outlet syndrome. Arch Surg 1989;
35 is level V expert opinion. 124(11):1335-1337.
addition to symptomatic improve-
References printed in bold type are 16. Takahara K, Uchiyama S, Nakagawa H,
ment. Recent literature suggests reli- Kamimura M, Ohashi M, Miyasaka T:
those published within the past 5
able improvement of symptoms can Snapping scapula syndrome due to
be achieved with open or arthro- years. malunion of rib fractures: A case report.
J Shoulder Elbow Surg 2004;13(1):
scopic techniques; however, complete 1. Bionet: Fait clinique. Bull Mem Soc Chir 95-98.
resolution of symptoms may not be Paris1867;8:458.
17. Manske RC, Reiman MP, Stovak ML:
achieved universally. Millett et al39 2. Aggarwal A, Wahee P, Harjeet, Nonoperative and operative
reported that although patients’ Aggarwal AK, Sahni D: Variable osseous management of snapping scapula. Am J
anatomy of costal surface of scapula and Sports Med 2004;32(6):1554-1565.
symptoms substantially improved its implications in relation to snapping
18. Fukunaga S, Futani H, Yoshiya S:
following arthroscopic procedures, scapula syndrome. Surg Radiol Anat
2011;33(2):135-140. Endoscopically assisted resection of a
outcome scores remained lower than scapular osteochondroma causing
expected. Similarly, Pearse et al28 3. Ciullo JV: Subscapular bursitis: snapping scapula syndrome. World J
Treatment of “snapping scapula” or Surg Oncol 2007;5:37.
noted that only six of nine patients “wash-board syndrome.” Arthroscopy
19. van Riet RP, Van Glabbeek F:
returned to their previous level of 1992;8:412-413.
Arthroscopic resection of a symptomatic
sport. 4. Kuhne M, Boniquit N, Ghodadra N, snapping subscapular osteochondroma.
Romeo AA, Provencher MT: The Acta Orthop Belg 2007;73(2):252-254.
snapping scapula: Diagnosis and
treatment. Arthroscopy 2009;25(11): 20. Cinar BM, Akpinar S, Derincek A, Beyaz
S, Uysal M: Elastofibroma dorsi: An
Summary 1298-1311.
unusual cause of shoulder pain
5. Cobey MC: The rolling scapula. Clin [Turkish]. Acta Orthop Traumatol Turc
Scapulothoracic bursitis and snap- Orthop Relat Res 1968;60:193-194. 2009;43(5):431-435.
ping scapula syndrome represent a 6. Percy EC, Birbrager D, Pitt MJ: 21. Edelson JG: Variations in the anatomy of
spectrum of disease with symptoms Snapping scapula: A review of the the scapula with reference to the
literature and presentation of 14 snapping scapula. Clin Orthop Relat Res
that range from mildly irritating to patients. Can J Surg 1988;31(4):248- 1996;(322):111-115.
debilitating. Nonsurgical therapy re- 250.
22. Arntz C, Matsen FI: Partial
mains the initial treatment of choice 7. Milch H: Snapping scapula. Clin Orthop scapulectomy for disabling
but appears to be less successful in 1961;20:139-150. scapulothoracic snapping. Orthop Trans
1990;14:252-253.
patients with anatomic scapulotho- 8. Sisto DJ, Jobe FW: The operative
treatment of scapulothoracic bursitis in 23. McCluskey G, Bigliani L: Surgical
racic abnormalities. If nonsurgical
professional pitchers. Am J Sports Med management of refractory
measures fail, surgical intervention, 1986;14(3):192-194. scapulothoracic bursitis. Orthop Trans
including open, arthroscopic, and 1991;15:801.
9. Codman E: The Shoulder. Malabar, FL,
combined techniques, have been suc- Krieger Publishing, 1984, pp 1-31. 24. Mozes G, Bickels J, Ovadia D, Dekel S:

April 2013, Vol 21, No 4 223


Snapping Scapula Syndrome: Diagnosis and Management

The use of three-dimensional computed snapping scapula syndrome. J Shoulder scapulothoracic disorders, in Miller M,
tomography in evaluating snapping Elbow Surg 2002;11(1):80-85. Cole B, eds: Textbook of Arthroscopy.
scapula syndrome. Orthopedics 1999; Philadelphia, PA, Saunders, 2004,
22(11):1029-1033. 31. Kibler WB, McMullen J: Scapular
pp 277-287.
dyskinesis and its relation to shoulder
25. Higuchi T, Ogose A, Hotta T, et al: pain. J Am Acad Orthop Surg 2003; 37. Frank DK, Wenk E, Stern JC, Gottlieb
Clinical and imaging features of 11(2):142-151. RD, Moscatello AL: A cadaveric study of
distended scapulothoracic bursitis: the motor nerves to the levator scapulae
Spontaneously regressed pseudotumoral 32. Pavlik A, Ang K, Coghlan J, Bell S:
Arthroscopic treatment of painful muscle. Otolaryngol Head Neck Surg
lesion. J Comput Assist Tomogr 2004;
snapping of the scapula by using a new 1997;117(6):671-680.
28(2):223-228.
superior portal. Arthroscopy 2003;19(6):
38. Chan BK, Chakrabarti AJ, Bell SN: An
26. Ken O, Hatori M, Kokubun S: The MRI 608-612.
alternative portal for scapulothoracic
features and treatment of
scapulothoracic bursitis: Report of four 33. Groh GI, Simoni M, Allen T, Dwyer T, arthroscopy. J Shoulder Elbow Surg
cases. Ups J Med Sci 2004;109(1):57-64. Heckman MM, Rockwood CA Jr: 2002;11(3):235-238.
Treatment of snapping scapula with a
27. Hodler J, Gilula LA, Ditsios KT, periscapular muscle strengthening 39. Millett PJ, Gaskill TR, Horan MP, van
Yamaguchi K: Fluoroscopically guided program. J Shoulder Elbow Surg 1996; der Meijden OA: Technique and
scapulothoracic injections. AJR Am J 5(2):S6. outcomes of arthroscopic
Roentgenol 2003;181(5):1232-1234. scapulothoracic bursectomy and partial
34. Williams GR Jr, Shakil M, Klimkiewicz scapulectomy. Arthroscopy 2012;28(12):
28. Pearse EO, Bruguera J, Massoud SN, J, Iannotti JP: Anatomy of the 1776-1783.
Sforza G, Copeland SA, Levy O: scapulothoracic articulation. Clin
Arthroscopic management of the painful Orthop Relat Res 1999;(359):237-246. 40. Lien SB, Shen PH, Lee CH, Lin LC: The
snapping scapula. Arthroscopy 2006; effect of endoscopic bursectomy with
22(7):755-761. 35. Millett P, Pacheco I, Gobezie R, Warner mini-open partial scapulectomy on
JJ: Management of recalcitrant snapping scapula syndrome. J Surg Res
29. Lehtinen JT, Macy JC, Cassinelli E, scapulothoracic bursitis: Endoscopic 2008;150(2):236-242.
Warner JJ: The painful scapulothoracic scapulothoracic bursectomy and
articulation: Surgical management. Clin scapuloplasty. Techniques in Shoulder 41. Lehtinen JT, Tetreault P, Warner JJ:
Orthop Relat Res 2004;(423):99-105. and Elbow Surgery 2006;7:200-205. Arthroscopic management of painful and
stiff scapulothoracic articulation.
30. Nicholson GP, Duckworth MA: 36. O’Holleran J, Millett P, Warner JJ: Arthroscopy 2003;19(4):E28.
Scapulothoracic bursectomy for Arthroscopic management of

224 Journal of the American Academy of Orthopaedic Surgeons


Review Article

Chondroblastoma and
Chondromyxoid Fibroma

Abstract
Camila B. R. De Mattos, MD Chondroblastoma and chondromyxoid fibroma are benign but
Chanika Angsanuntsukh, MD locally aggressive bone tumors. Chondroblastoma, a destructive
lesion with a thin radiodense border, is usually seen in the
Alexandre Arkader, MD
epiphysis of long bones. Chondromyxoid fibroma presents as a
John P. Dormans, MD bigger, lucent, loculated lesion with a sharp sclerotic margin in the
metaphysis of long bones. Although uncommon, these tumors can
be challenging to manage. They share similarities in pathology that
could be related to their histogenic similarity. Very rarely,
From the Department of chondroblastoma may lead to lung metastases; however, the
Orthopaedic Surgery, The Children’s
Hospital of Philadelphia, mechanism is not well understood.
Philadelphia, PA (Dr. De Mattos and
Dr. Dormans), the Department of
Orthopaedic Surgery, Ramathibodi
Hospital, Mahidol University,
Bangkok, Thailand
(Dr. Angsanuntsukh), Children’s
C hondroblastoma is a rare, be-
nign bone tumor, usually lo-
cated in the epiphysis or apophysis
Epidemiology

Hospital Los Angeles, Los Angeles, Chondroblastoma represents 1% to


CA (Dr. Arkader), and the University of long bones. It was first described
2% of all primary bone tumors and
of Pennsylvania School of Medicine, by Kolodny in 1927 as a cartilage-
Philadelphia (Dr. Dormans).
approximately 5% of benign bone
containing giant cell tumor (GCT)
tumors.4-6 The ratio of male to fe-
Dr. Arkader or an immediate family but was better characterized by Cod-
male patients is approximately
member serves as a paid consultant man in 1931, who believed it to be
to or is an employee of Biomet 2:1.4,5,7-10 Although chondroblastoma
an “epiphyseal chondromatous giant
Trauma. Dr. Dormans or an has been reported in patients ranging
immediate family member serves as cell tumor” involving the proximal
in age from 2 to 73 years, most pa-
a board member, owner, officer, or humerus.1 In 1942, Jaffe and Lich- tients are aged <20 years.7-9,11,12
committee member of the Pediatric tenstein,2 after a comprehensive re-
Orthopaedic Society of North The bone most affected by chon-
America, the Scoliosis Research view, included tumors in locations
droblastoma is the femur, followed
Society, the International Society of other than the proximal humerus
by the humerus and tibia.7,9-12 Re-
Orthopaedic Surgery and and designated the tumor as benign
Traumatology (SICOT) Foundation, ports in the literature fluctuate be-
chondroblastoma of bone, that is, as
SICOT USA, and the World tween identifying the proximal hu-
Orthopaedic Concern. Neither of the a different, separate entity from merus and proximal femur as the
following authors or any immediate GCT. Historically, because of Cod- most affected site.7-9,11,12 In the foot,
family member has received man’s great contribution, chondro-
anything of value from or has stock chondroblastoma is located espe-
or stock options held in a blastoma of the proximal humerus cially in the talus and calcaneus, in
commercial company or institution was referred as “Codman tumor.” an apophysis or near the articular
related directly or indirectly to the
subject of this article: Dr. De Mattos
Chondromyxoid fibroma (CMF), a surface.13 Chondroblastoma can also
and Dr. Angsanuntsukh. rare mixture of benign cartilage and fi- occur in flat bones, such as the scap-
J Am Acad Orthop Surg 2013;21:
brous and myxoid tissue that generally ula, patella, sternum, and skull
225-233 develops in long bones of the lower ex- bones.5 The average age of patients
tremity, was described in 1948 by Jaffe with chondroblastoma in small or
http://dx.doi.org/10.5435/
JAAOS-21-04-225 and Lichtenstein.3 Prior to their de- flat bones is higher than that of pa-
scription, the lesion was thought to tients with chondroblastoma of long
Copyright 2013 by the American
Academy of Orthopaedic Surgeons. be a myxoma of the bone, enchon- bones.6,13 About 0.5% to 1% of
droma, or chondrosarcoma. chondroblastomas present on verte-

April 2013, Vol 21, No 4 225


Chondroblastoma and Chondromyxoid Fibroma

Figure 1 mors, there is no single characteristic borders. The cells contain one or two
abnormality or chromosomal break- round, oval, slightly indented, or
ing point specific for chondroblas- even multilobulated nuclei with or
toma or CMF. without nucleoli.8 Occasional cells
The histogenesis of chondroblas- may have enlarged nuclei without
toma and CMF is still uncertain. Ro- nuclear atypia.4,25 The presence of
meo et al20 confirmed the active role mitotic figures is scarce.2,4,25 There
of cartilage-signaling molecules, both are scattered multinucleated osteo-
Indian Hedgehog/parathyroid hor- clast-type giant cells among the
mone–related protein (IHh/PTHrP) chondroblasts.7,8 There may be foci
and fibroblast growth factor, indicat- of chondroid matrix formed by the
ing that chondroblastoma is a neo- chondroblasts.25 Dystrophic calcifi-
Photomicrograph of
chondroblastoma. Note the diffuse plasm that originates from a mesen- cation is occasionally present and
and compact proliferation of chymal cell committed toward may surround individual cells, giving
mononuclear cells with indented chondrogenesis via active growth the classic “chicken wire” appear-
nuclei with abundant eosinophilic
plate signaling pathways. This con- ance7,8 (Figure 1), although this is
cytoplasm and distinct cell borders.
There is presence of focal clusion supports the chondrogenic not mandatory for diagnosis.
pericellular (ie, chicken wire) nature of this tumor and the close re- In 15% to 32% of cases, chondro-
calcification (arrows) on the top left lationship between the physis and blastoma may be associated with
corner (hematoxylin-eosin, original
magnification ×400). the tumor.21 CMF has myofibroblas- secondary aneurysmal bone cyst
tic differentiation in its “fibrous” ar- (ABC).7-9,11 Although the reasons for
eas driven by transforming growth this association are unclear, hypothe-
brae, generally in the posterior ele-
factor β-1.22 A strong expression of ses include mechanical stress,
ments and/or the body.14
the Sox9 gene, which is responsible trauma, and hemorrhage.13 More ag-
A prevalence of <0.5% of all bone tu-
for chondrocytic differentiation as gressive chondroblastoma that can
mors is reported in many series describ-
well as regulation of the expression cause metastases or recurrence shows
ing CMF.6,15,16 There is a slight male
of cartilage-specific genes in mature no difference in histology compared
predominance.17 CMF most com-
chondrocytes, especially the synthe- with less aggressive chondroblas-
monly arises in young patients in the
sis of collagen type II, was found in toma.25 The histology is equivalent
second or third decades of life.3,17,18
both chondroblastoma and CMF.23,24 to that of the primary site, and the
Most of these tumors are located in
This demonstrates that the expres- presence of atypical cells is rare.25
the metaphysis of long bones with
sion of Sox9 in these tumors is con- Grossly, CMF appears as lobulated,
variable distances from growth plate,
sistent with its commitment to the well-circumscribed, and sharply demar-
mainly in lower extremities.17 Rarely,
early phases of cartilage differentia- cated from the adjacent bone marrow.
the lesion involves the epiphysis. The
tion, with chondroblastoma being a The lesion is firm and white. The cut
diaphysis can be involved, especially
more “immature” tumor than CMF surface shows a solid tumor mass that
in large tumors. A lesion in small
because of the greater presence of is yellow, grayish-white, or blue-
bones, such as phalanges, may in-
positive Sox9 in CMF cells.23 gray.6 Microscopic analysis of CMF
volve the bone in its totality. The
reveals three components: myxoma-
proximal tibia is the most common
tous zones, fibrous zones, and fields
site, comprising 28% to 52% of all
Pathology that appear chondroid. The classic
lower extremity lesions in the litera-
histologic features of CMF are lob-
ture.17,19 This site is followed by the
Grossly, a chondroblastoma is a ules of stellate or spindle-shaped cells
ilium, ribs, distal femur, metatarsals,
gray-white tumor with yellowish ar- in abundant myxoid background or
and distal tibia.17 In contrast to
eas, usually because of calcification, chondroid intercellular material.
chondroblastoma, CMF is rarely en-
which can be soft, rubbery, or fria- Scattered giant cells are found in ap-
countered in the humerus.15,17
ble.2 Microscopically, chondroblas- proximately 50% of cases, usually at
toma reveals proliferation of mono- the edge of the lobules16,17 (Figure 2).
Etiology nuclear cells.10 The tumor is These lobules have a hypocellular
characterized by compact areas of center and a condensation of the nu-
Although cytogenetic abnormalities round, oval, or polygonal chondro- clei toward the periphery, creating a
can be highly specific for some tu- blasts with well-defined cytoplasmic hypercellular periphery. The inter-

226 Journal of the American Academy of Orthopaedic Surgeons


Camila B. R. De Mattos, MD, et al

Figure 2 Figure 3

Photomicrograph of chondromyxoid
fibroma. Note the stellate cells in a
myxoid background. The stellate
cells display mild atypia, but
mitoses are rarely seen. The lesion AP (A) and AP with internal rotation (B) radiographs of a chondroblastoma of
has a lobulated appearance, with the proximal humerus of a 15-year-old girl who presented with right shoulder
alternating cellular and mode pain lasting 4 months. The lesion is located entirely in the epiphysis, is
myxoid areas (hematoxylin-eosin, lucent, and has thin, sclerotic borders.
original magnification ×200).

lobular tissue is composed of oval or be present, if the patient has had


spindle-shaped cells. Clinical Presentation symptoms for several years, because
Mitotic features are uncommon of expansion of the lesion.28 Patho-
and are usually present in more con- Chondroblastoma and CMF are usu-
logic fractures in long bones are not
centrated cellular interlobular areas. ally classified, using the Enneking be-
common at presentation, but when
Atypical mitotic features are not nign bone tumor classification, as
the lesion is in the foot, subchondral
found, although some cells are large stage 2 (ie, active) or 3 (ie, aggres-
fracture is frequent and painful.13
and have irregularities in the size and sive). The delay between the onset of
CMF may be found incidentally
shape of nuclei.17 Cellular atypia was symptoms and diagnosis varies from
but more often presents with pain
reported in 18% of cases by Wu <1 month to years. Although presen-
that is usually intermittent and not
et al;17 however, there was no change tation of these tumors can be similar,
distressing. The duration of symp-
in the nucleocytoplasmic ratio. Le- chondroblastoma is typically more
toms ranges from several months to
sions in hands and feet are more painful than CMF.
years. The second most common pre-
likely to have atypical cells.17 Chondroblastoma normally has an sentation is local swelling, a lump, or
Myxoid stroma in CMF stains insidious presentation. Symptoms a palpable mass. The patient may
uniformly and does not show exten- vary from mild to significant pain present with pain to palpation, and
sive liquefaction, as is present in and the presence of a soft-tissue mass the lump may slowly increase in size.
myxoid foci of chondrosarcoma. or even a pathologic fracture. Pa- The local swelling or lump is more
Nevertheless, small foci of liquefac- tients with chondroblastoma may re- common in tumor of the small
tive changes are found in approxi- port pain lasting for several weeks, bones. Limping, limitation of adja-
mately 30% of CMF cases.6 months, or even years. Pain with lo- cent joint range of motion, and
Cyst formation, necrosis, foam cal tenderness in the involved bone pathologic fracture are rare.3,6,15,19,29,30
cells, foci of secondary ABC, and and the adjacent joint is the most fre-
frank hyaline cartilaginous areas are quent complaint, followed by de-
unusual findings.6,17 Calcifications creased range of motion.4,5,8,10-12 Radiologic Evaluation
are present in approximately one Some patients attribute the pain to
third of the lesions and appear as trauma, usually a minor or sports- The classic radiographic appearance
fine lacelike or plaquelike deposits.6 related injury.7 Swelling or joint effu- of chondroblastoma is a well-defined
Histochemical analysis of chondro- sion, a limp (when the affected bone eccentric oval or round lytic lesion
blastoma and CMF demonstrates is in the lower extremity), and mus- involving the epiphysis adjacent to
great positivity to collagen type II cle wasting may also be seen.5,7,10,12 A an open growth plate4 (Figure 3). A
and S-100 protein.8,10,24,26,27 palpable mass is uncommon but may sharp sclerotic margin is often seen.

April 2013, Vol 21, No 4 227


Chondroblastoma and Chondromyxoid Fibroma

Figure 4

Curettage and bone grafting of a chondroblastoma of the distal femur in an 11-year-old girl with chronic knee pain.
A, Preoperative AP radiograph demonstrating a lytic lesion on the distal femur that extends from the epiphysis into the
metaphysis. B, Sagittal T1-weighted magnetic resonance image demonstrating peripheral lobulation and associated
marrow edema. C, Intraoperative AP fluoroscopic image demonstrating curettage and bone grafting of the lesion
performed through a cortical window, thereby avoiding damage to the unaffected surrounding physis. D, AP radiograph
made at 7-month follow-up. The patient was asymptomatic, with no complications or recurrence.

At times, the lesion may be mottled from the epiphyseal lesion.21 A few scan shows increased uptake but sel-
or fuzzy or contain areas of calcifica- case reports of diaphyseal chondro- dom is needed for diagnosis.21
tion. Lesion size on radiograph var- blastoma have appeared in the litera- CMF classically presents as a lytic
ies, with most being <4 cm.2,5,8,11 Cal- ture.34 Chondroblastomas located on radiolucent medullary lesion with a
cifications are found especially in small bones may be more aggressive, thin sclerotic rim (Figure 6). In most
skeletally immature patients.7 with loss of cortical continuity and lesions, borders are sharp, with par-
It is uncommon to find periosteal bony destruction.35 tial or complete effacement of the
bone formation on radiographs, but CT can help define the anatomic cortex.16,17,29,36 CMF tends to be ec-
MRI usually depicts edema adjacent limits of the lesion, especially the dis- centrically located in the metaphysis
to the periosteum.31 In rare cases, es- tance to the growth plate and the re- of long bones. Rarely, or in advanced
pecially in older or neglected pa- lation of the lesion to subchondral cases, the lesion crosses the growth
tients, chondroblastoma may have bone. CT shows stipple calcification plate into epiphysis or extends into
an atypical presentation that clini- of the cartilaginous matrix, when the diaphysis.6 In small bones, CMF
cally and radiographically mimics an present. In addition, CT is useful in generally occupies the entire width of
aggressive process.5,28,32 delimiting lesions in unusual loca- the bone, causing thinning of cortices
The small percentage of chondro- tions as well as subchondral frac- and fusiform expansion of the bone.
blastomas with a secondary ABC in tures not visible on plain radio- The tumor typically has a scalloped
the histology usually show differ- graphs.13,14 border that is well defined by a nar-
ences from regular chondroblastoma In a few cases in which MRI was row rim of sclerotic bone. Chronic
on radiograph, and these sometimes not used in conjunction with radio- bone reaction and cortical thickening
lead to confusion in the diagnosis. graphs and the clinical presentation, are commonly present. Unusual peri-
Cystic changes are seen more com- this modality led to misdiagnosis or osteal reaction has been re-
monly when the lesion is located in overestimation of tumor aggressive- ported.16,17,36 Pseudotrabeculation,
bone, such as the patella.13,33 ness.31 Chondroblastoma usually is that is, ridges of the sclerotic rim at
Most chondroblastomas involve hypointense on T1-weighted images the edge of the lesion, is present.
the epiphysis of long bones.6 A small and variably ranges from hypoin- Gross and microscopic studies show
lesion is usually confined to a part of tense to hyperintense on T2- that there is no complete bony sep-
the epiphysis or apophysis, although weighted images, with or without tum.16
it may extend through the epiphyseal peripheral lobulation and the associ- Unlike other cartilaginous tumors,
plate21 (Figure 4). True metaphyseal ated marrow and soft-tissue edema calcification in CMF is unusual. The
chondroblastoma is rare; most re- that enhances after administration of prevalence of calcification in CMF
ported cases are of an extension contrast material31 (Figure 5). Bone ranges from 2.4% to 16% of cases

228 Journal of the American Academy of Orthopaedic Surgeons


Camila B. R. De Mattos, MD, et al

Figure 5 with staging and preoperative plan-


ning30 (Figure7).

Differential Diagnosis
The differential diagnosis for chon-
droblastoma includes GCT, simple
bone cyst, ABC, enchondroma, eo-
sinophilic granuloma, fibrous dys-
plasia, clear cell chondrosarcoma,
subacute osteomyelitis (ie, Brodie ab-
scess), and, when a subchondral cyst
is present, Legg-Calvé-Perthes dis-
ease or osteochondritis dissecans.
Tuberculosis can mimic the periartic-
The same patient as in Figure 3. Postcontrast T1-weighted fat-suppressed
ular pain and bone lesion of chon-
coronal (A) and T2-weighted axial (B) magnetic resonance images
demonstrating heterogeneously increased signal. The bone marrow is droblastoma and should be consid-
normal. ered, especially in developing
countries.6,8,21,25
The differential diagnosis for CMF
Figure 6
includes benign lesions such as GCT,
simple bone cyst, ABC, enchondroma,
eosinophilic granuloma, fibrous dys-
plasia, osteoblastoma, osteofibrous
dysplasia, and nonossifying fibro-
mas.6,18 Malignant conditions that
must be differentiated are low-grade
chondrosarcoma and myxoid chon-
drosarcomas.

Management
The natural history of these tumors
is not completely understood; to
date, there has been no evidence of
potential spontaneous healing.7 Sur-
gical management is advised for both
types of tumors because no effective
medical management is available.
AP (A) and lateral (B) radiographs of the proximal tibia of a 22-year-old man Both chondroblastoma and CMF
with chondromyxoid fibroma who presented with mild pain of the left knee
lasting for 3 months. Note the mild expansion of the tumor and the scalloped generally have a favorable prognosis
borders defined by thin sclerotic bone. Biopsy was performed, and the when identified and managed appro-
diagnosis was confirmed. (Adapted and printed with permission from priately.
Dr. Olavo Pires de Carvalho, University of São Paulo, São Paulo, Brazil.)
The benchmark management of
chondroblastoma is curettage with
radiologically, and from 6.8% to MRI are the preferred imaging mo- bone grafting.8-12,25 The entire tumor
34% of cases histologically.16,36 Cal- dalities. CT demonstrates cortical in- should be excised, with the surgeon
cification presents more often in pa- tegrity and calcification of the matrix following meticulous oncologic crite-
tients aged >40 years and in flat well. MRI shows low signal on T1- ria of a thorough intralesional exci-
bones.36 Pathologic fractures may be weighted images and increased signal sion through a cortical and/or epi-
found but are unlikely.17 CT and on T2-weighted images and can help physeal window (Figure 4), avoiding

April 2013, Vol 21, No 4 229


Chondroblastoma and Chondromyxoid Fibroma

Figure 7 droblastoma was recently described


in a small series.42 Results were best
with small tumors (approximately
1.5 cm) and when location of the tu-
mor provided limited risk of me-
chanical collapse of the adjacent ar-
ticular surface. Limited data support
this method of management, how-
ever, so patients must be selected
carefully.42
Some tumors can be widely ex-
cised, especially in bones such as ribs
and fibula.9,10 Lin et al9 reported no
recurrence in all six patients in
whom chondroblastoma was treated
through en bloc resection.
Aggressive recurrences historically
treated with amputation can now be
managed with limb-sparing tech-
niques and endoprosthetic recon-
Sagittal T1-weighted fat-suppressed (A) and coronal T2-weighted struction, if feasible.5,12
postcontrast (B) magnetic resonance images of a chondromyxoid fibroma of No clear guideline exists for fol-
the distal phalanx of the great toe, demonstrating edema in the soft tissue lowing patients with chondroblas-
and an expansive and solid lesion surrounded by a thin shell of residual toma. The risk of late recurrence and
bone. There is intralesional calcification with discrete contrast enhancement
in the periphery of the lesion, characteristic of cartilaginous lesions. lung metastases, although extremely
low, argues for prudent follow-up.
Lin et al9 suggested following pa-
the growth plate with the help of in- of malignant transformation.5,7,38 tients on a yearly basis for at least 5
traoperative fluoroscopy.9,10 Curet- Management of a lesion in the years.9 Plain chest radiographs made
tage through the physis with obliter- femoral head is challenging because preoperatively and at the annual visit
ation of part or all of the growth of the difficulty of access—more so if are recommended.
plate is an option in patients who are the epiphysis is not fused.10,33 The Because CMF is extremely rare,
near the end of skeletal growth.9 traditional approach for this lesion is most published articles are from se-
Intra-articular exposure should be through the base of the femoral neck ries with patients who were treated
considered to access all of the tumor, or the trochanter, although a direct over several decades; thus, there are no
if necessary. hip approach can also be used.7,12 ultimate recommendations for manage-
Lehner et al37 noted insufficient ev- Both techniques carry the risk of ment. The options include curettage
idence supporting the use of adju- spreading tumor into the femoral and excision, with or without filling of
vant therapy. A high-speed burr is neck or the hip joint as well as of the cavitary defect. Wide resection or
useful, with caution exercised near damaging the growth plate.10,33 The en bloc excision is probably the best
the growth plate and subchondral use of arthroscopy to visually inspect method to avoid recurrence, but not all
bone.9,37 Electrocautery, phenol, ar- the cavity following curettage via a locations allow the mechanical imbal-
gon bean coagulation, and cryother- minimally invasive approach, similar ance these procedures can cause, so
apy also may be used with cau- to core decompression, without com- bone grafting is advised.6,18 CMF can
tion.5,9,11,37 Bone graft is the preferred promising the articular cartilage of be locally aggressive; thus, adjuvants
material to fill the cavitary defect af- the adjacent joint, has been success- such as PMMA are recommended (Fig-
ter curettage.9,10 In a series of 47 pa- ful, although reported in only case ure 8). Curettage alone has resulted in
tients, Ramappa et al11 reported no reports.33,39,40 A trapdoor procedure a rate of high recurrence in most
recurrence of tumor in 8 patients has also been described, but it can series.16-18,29 Many authors report
treated with polymethyl methacry- result in osteonecrosis and perma- that bone grafting after excisional
late (PMMA). Radiotherapy is pro- nent damage to the cartilage.12,33,41 curettage reduces the recurrence rate,
scribed because of the increased risk Radiofrequency ablation for chon- with some stating that the rate is

230 Journal of the American Academy of Orthopaedic Surgeons


Camila B. R. De Mattos, MD, et al

Figure 8 complete excision.7,9,11,12


Some authors have postulated that
pelvic chondroblastoma may be
more biologically aggressive than
other forms of chondroblastoma.5,9,11
Recurrences can occur between 5
months to 7 years after the initial
procedure (average, 10 months fol-
lowing diagnosis).7,9,12 Recurrence is
not related to one specific mode of
management, tumor size, patient sex,
or duration of follow-up.8,10,11 de
Silva and Reid8 reported a statisti-
cally significant relation between du-
ration of symptoms and recurrence.
They stated that patients with symp-
toms of <6 months had a greater
chance of recurrence; however, to
A, Intraoperative photograph demonstrating anterior access to the proximal our knowledge, this has not been re-
tibia, allowing extensive curettage through a cortical window of the ported by other authors. Suneja
chondromyxoid fibroma shown in Figure 6. B, Intraoperative photograph
demonstrating the cavity packed with polymethyl methacrylate. (Adapted and et al12 described a positive associa-
printed with permission from Dr. Olavo Pires de Carvalho, University of São tion of young age and higher recur-
Paulo, São Paulo, Brazil.) rence rate, although this, too, has
not been noted by others.7,9 The as-
sociation of chondroblastoma with
similar to that observed after resec- Sarcomatous change has been re-
ABC was reported by Huvos and
tion.6,18 Use of PMMA as an adju- ported in some series of CMF pa-
Marcove43 to have a higher recur-
vant after excisional curettage re- tients, but the prevalence is very
rence rate; this association was re-
portedly decreases the rate of low.6,17
futed later by others.7,9,11,12 Recur-
recurrence.18
rence of chondroblastoma in the soft
Recurrence tissue surrounding the treated lesion
Complications is believed to occur because of im-
The recurrence rates of chondroblas- plantation or incomplete curettage
Recurrence of the lesion is the most toma vary from 5% to 40%; study and the subsequent growth of the re-
common complication following man- results are inconclusive in determin- sidual tumor cells, especially when
agement of chondroblastoma and ing which patients have greater the affected joint capsule was
CMF. Although growth disturbances chances of recurrence.9,10,12 Most re- opened.25 In sum, then, recurrence of
may occur following the resection of cent series report rates of 8% to chondroblastoma depends funda-
these lesions because of their proxim- 13%.9,10,12 The recurrence rate for mentally on incomplete resection and
ity to the physis, major angular defor- CMF ranges from 20% to 25%.16,18 biologic aggressiveness.9
mities and discrepancies are not Some authors state that recurrence Lesions that contain enlarged and
common.9,11,12,33 in chondroblastoma arises more irregular nuclei or have a prominent
Functional impairment, degenera- commonly in patients with an open myxoid matrix are more likely to re-
tive joint disease, and pathologic epiphyseal plate, but others contra- cur in CMF.16 The type of manage-
fractures can also result.11,33 Suneja dict this finding.7-12 Recurrence in ment, however, is the most important
et al12 described a series of 40 pa- skeletally immature patients can be factor that affects the rate of recur-
tients with chondroblastoma treated explained by inadequate curettage rence of this tumor. Curettage alone
with curettage and bone graft with done to avoid damage to the growth results in a very high recurrence rate
an average Musculoskeletal Tumor plate.7,10 The proximal femur and in many series; Lersundi et al18 re-
Society functional evaluation of pelvis have higher rates of recur- ported that a recurrence rate of 38%
94.2%. The higher-scoring patients rence, likely related to difficulty in after curettage alone diminished to
had lesions in more accessible areas. accessing these sites and obtaining 13% when the cavitary defect was

April 2013, Vol 21, No 4 231


Chondroblastoma and Chondromyxoid Fibroma

filled with bone graft. Of the 29 pa- those published within the past 5
tients with CMF in their study, there Summary years.
was no recurrence in the 3 who un-
Chondroblastoma and CMF are un- 1. Codman EA: The Classic: Epiphyseal
derwent curettage plus PMMA or chondromatous giant cell tumors of the
common benign bone tumors that upper end of the humerus. Surg Gynecol
the 4 who were treated with wide re-
present with insidious bone pain. Obstet.1931;52:543. Clin Orthop Relat
section. Res 2006;450:12-16.
Chondroblastoma usually involves
the epiphysis or apophysis of long 2. Jaffe HL, Lichtenstein L: Benign
chondroblastoma of bone: A
bones; CMF is a metaphyseal tumor. reinterpretation of the so-called
Metastasis The radiographic appearance of calcifying or chondromatous giant cell
chondroblastoma is of a lytic lesion tumor. Am J Pathol 1942;18(6):969-991.
Metastases from chondroblastoma
can arise from different primary with sclerotic borders. CMF is also 3. Jaffe HL, Lichtenstein L: Chondro-
myxoid fibroma of bone: A distinctive
sites. There is no reported relation of radiolucent with a sclerotic border, benign tumor likely to be mistaken espe-
metastasis to previous surgery or but it is usually larger than CMF and cially for chondrosarcoma. Arch Pathol
can have a bubbly appearance. Peri- (Chic) 1948;45(4):541-551.
nonsurgical treatment, tumor loca-
tion, or patient age.25,44,45 The inci- osteal reaction is uncommon for 4. Schajowicz F, Gallardo H: Epiphysial
chondroblastoma of bone: A clinico-
dence of metastases associated with both tumors. The chance of recur- pathological study of sixty-nine cases.
chondroblastoma is not known but rence of chondroblastoma is 8% to J Bone Joint Surg Br 1970;52(2):205-
13% and, for CMF, 20% to 25%. 226.
is thought to be very low. Rodgers
and Mankin46 described 2 patients of Surgical management can be chal- 5. Dahlin DC, Ivins JC: Benign
chondroblastoma: A study of 125 cases.
80 (2.5%) with chondroblastomas lenging because, especially in young
Cancer 1972;30(2):401-413.
treated for metastases at their institu- patients with chondroblastoma, the
6. Unni KK, Inwards CY: Chondromyxoid
tion. Selection bias can probably ex- ideal is to avoid the chance of recur- fibroma, in Unni KK, Inwards CY, eds:
plain this elevated rate; most authors rence while preserving the integrity Dahlin’s Bone Tumors, ed 6.
Philadelphia, PA, Wolters Kluwer,
believe it to be <1%.45 To date, there of the physis. Metastases are very
Lippincott Williams & Wilkins, 2010, pp
has been no published study on me- uncommon and have a good progno- 50-59.

tastases from CMF. sis when they are resectable. Addi- 7. Springfield DS, Capanna R, Gherlinzoni
tional genetic studies can likely help F, Picci P, Campanacci M: Chondro-
The lung is by far the most common blastoma: A review of seventy cases.
identify the cause of metastases and
site of distant metastases. Bones differ- J Bone Joint Surg Am 1985;67(5):748-
explain the nature of the aggressive 755.
ent from those of the primary site, soft
chondroblastoma. 8. de Silva MV, Reid R: Chondroblastoma:
tissue, the skin, and the liver are also
Varied histologic appearance, potential
cited.11,25,44 The time reported for me- diagnostic pitfalls, and clinicopathologic
tastases to manifest clinically ranges features associated with local recurrence.
Acknowledgments Ann Diagn Pathol 2003;7(4):205-213.
5 months to 33 years (average, 8
years) from the initial diagnosis of The authors would like to thank 9. Lin PP, Thenappan A, Deavers MT,
Lewis VO, Yasko AW: Treatment and
chondroblastoma.25,46 Olavo Pires de Carvalho, MD, and prognosis of chondroblastoma. Clin
Ostrowski et al47 reported evidence Marta E. Gutemberg, MD, for al- Orthop Relat Res 2005;438:103-109.
of p53 mutation in one patient with lowing the use of photographs of 10. Sailhan F, Chotel F, Parot R; SOFOP:
chondroblastoma and metastases. In their cases for this article. Chondroblastoma of bone in a pediatric
population. J Bone Joint Surg Am 2009;
contrast, Hasegawa et al27 found no 91(9):2159-2168.
evidence of p53 mutation in any of
11. Ramappa AJ, Lee FY, Tang P, Carlson
five patients with chondroblastoma References JR, Gebhardt MC, Mankin HJ:
without metastases. The p53 muta- Chondroblastoma of bone. J Bone Joint
Evidence-based Medicine: Levels of Surg Am 2000;82(8):1140-1145.
tion is a late event in tumorigenesis
and is present in many high-grade evidence are described in the table of 12. Suneja R, Grimer RJ, Belthur M, et al:
Chondroblastoma of bone: Long-term
sarcomas, including osteosarcomas contents. In this article, references results and functional outcome after
and chondrosarcomas.47 1-5, 7-12, 14-24, 26, 27, 30, 31, 33, intralesional curettage. J Bone Joint Surg
35-39, and 42 are level IV studies. Br 2005;87(7):974-978.
Patients usually survive several
years with metastatic lesions; the References 25, 29, 32, 34, 40, 41, 13. Fink BR, Temple HT, Chiricosta FM,
Mizel MS, Murphey MD: Chondro-
prognosis is better when the metasta- and 43-45 are level V expert opin- blastoma of the foot. Foot Ankle Int
ses are resectable.25,44 There is no re- ion. 1997;18(4):236-242.
ported benefit from chemotherapy.25 References printed in bold type are 14. Ilaslan H, Sundaram M, Unni KK:

232 Journal of the American Academy of Orthopaedic Surgeons


Camila B. R. De Mattos, MD, et al

Vertebral chondroblastoma. Skeletal Report of a fatal case with a review of calcification in chondromyxoid fibroma.
Radiol 2003;32(2):66-71. the literature on atypical, aggressive, and Skeletal Radiol 1998;27(10):559-564.
malignant chondroblastoma. Cancer
15. Dahlin DC: Chondromyxoid fibroma of 1985;55(8):1770-1789. 37. Lehner B, Witte D, Weiss S: Clinical and
bone, with emphasis on its morpho- radiological long-term results after
logical relationship to benign chondro- 26. Park HR, Park YK, Jang KT, Unni KK: operative treatment of chondroblastoma.
blastoma. Cancer 1956;9(1):195-203. Expression of collagen type II, S100B, Arch Orthop Trauma Surg 2011;131(1):
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16. Rahimi A, Beabout JW, Ivins JC, Dahlin blastoma and chondromyxoid fibroma.
DC: Chondromyxoid fibroma: A Oncol Rep 2002;9(5):1087-1091. 38. Copeland MM, Geschickter CF:
clinicopathologic study of 76 cases.
Chondroblastic tumors of bone: Benign
Cancer 1972;30(3):726-736. 27. Hasegawa T, Seki K, Yang P, et al:
and malignant. Ann Surg 1949;129(5):
Differentiation and proliferative activity
17. Wu CT, Inwards CY, O’Laughlin S, 724-733.
in benign and malignant cartilage tumors
Rock MG, Beabout JW, Unni KK: of bone. Hum Pathol 1995;26(8):838-
Chondromyxoid fibroma of bone: A 39. Thompson MS, Woodward JS Jr: The
845. use of the arthroscope as an adjunct in
clinicopathologic review of 278 cases.
Hum Pathol 1998;29(5):438-446. 28. Kirchhoff C, Buhmann S, Mussack T, the resection of a chondroblastoma of
et al: Aggressive scapular chondro- the femoral head. Arthroscopy 1995;
18. Lersundi A, Mankin HJ, Mourikis A, blastoma with secondary metastasis: A 11(1):106-111.
Hornicek FJ: Chondromyxoid fibroma: case report and review of literature. Eur
A rarely encountered and puzzling 40. Stricker SJ: Extraarticular endoscopic
J Med Res 2006;11(3):128-134.
tumor. Clin Orthop Relat Res 2005;439: excision of femoral head
171-175. 29. Sharma H, Jane MJ, Reid R: chondroblastoma. J Pediatr Orthop
Chondromyxoid fibroma of the foot and 1995;15(5):578-581.
19. Baker AC, Rezeanu L, O’Laughlin S, ankle: 40 years’ Scottish bone tumour
Unni K, Klein MJ, Siegal GP: registry experience. Int Orthop 2006; 41. Iwai T, Abe S, Miki Y, et al: A trapdoor
Juxtacortical chondromyxoid fibroma of 30(3):205-209. procedure for chondroblastoma of the
bone: A unique variant. A case study of femoral head: A case report. Arch
20 patients. Am J Surg Pathol 2007; 30. Armah HB, McGough RL, Goodman Orthop Trauma Surg 2008;128(8):763-
31(11):1662-1668. MA, et al: Chondromyxoid fibroma of 767.
rib with a novel chromosomal
20. Romeo S, Bovée JV, Jadnanansing NA, translocation: A report of four additional 42. Rybak LD, Rosenthal DI, Wittig JC:
Taminiau AH, Hogendoorn PC: cases at unusual sites. Diagn Pathol Chondroblastoma: Radiofrequency
Expression of cartilage growth plate 2007;2:44. ablation. Alternative to surgical resection
signalling molecules in chondroblastoma.
in selected cases. Radiology 2009;
J Pathol 2004;202(1):113-120. 31. Weatherall PT, Maale GE, Mendelsohn
DB, Sherry CS, Erdman WE, Pascoe HR: 251(2):599-604.
21. Maheshwari AV, Jelinek JS, Song AJ, Chondroblastoma: Classic and confusing
Nelson KJ, Murphey MD, Henshaw 43. Huvos AG, Marcove RC: Chondro-
appearance at MR imaging. Radiology blastoma of bone: A critical review. Clin
RM: Metaphyseal and diaphyseal 1994;190(2):467-474.
chondroblastomas. Skeletal Radiol Orthop Relat Res 1973;95:300-312.
2011;40(12):1563-1573. 32. Kim J, Kumar R, Raymond AK, Ayala
44. Khalili K, White LM, Kandel RA,
AG: Non-epiphyseal chondroblastoma
22. Romeo S, Eyden B, Prins FA, Briaire-de Wunder JS: Chondroblastoma with
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Bruijn IH, Taminiau AH, Hogendoorn by an aneurysmal bone cyst: A case multiple distant soft tissue metastases.
PC: TGF-beta1 drives partial report and review of the literature. Skeletal Radiol 1997;26(8):493-496.
myofibroblastic differentiation in Skeletal Radiol 2010;39(6):583-587.
chondromyxoid fibroma of bone. 45. Joshi DD, Anderson PM, Matsumoto J,
J Pathol 2006;208(1):26-34. 33. Strong DP, Grimer RJ, Carter SR, et al: Metastatic chondroblastoma with
Tillman RM, Abudu A: Chondro- elevated creatine kinase and
23. Dancer JY, Henry SP, Bondaruk J, et al: blastoma of the femoral head: Manage- paraneoplastic neurologic autoimmunity.
Expression of master regulatory genes ment and outcome. Int Orthop 2010; J Pediatr Hematol Oncol 2003;25(11):
controlling skeletal development in 34(3):413-417. 900-904.
benign cartilage and bone forming
tumors. Hum Pathol 2010;41(12):1788- 34. Azorín D, González-Mediero I, 46. Rodgers WB, Mankin HJ: Metastatic
1793. Colmenero I, De Prada I, López-Barea F: malignant chondroblastoma. Am J
Diaphyseal chondroblastoma in a long Orthop (Belle Mead NJ) 1996;25(12):
24. Konishi E, Nakashima Y, Iwasa Y, bone: First report. Skeletal Radiol 2006; 846-849.
Nakao R, Yanagisawa A: Immuno- 35(1):49-52.
histochemical analysis for Sox9 reveals 47. Ostrowski ML, Johnson ME, Truong
the cartilaginous character of chondro- 35. Tarkkanen M, Karaharju E, Böhling T, LD, Hicks MJ, Smith FE, Spjut HJ:
blastoma and chondromyxoid fibroma et al: Chromosome study of 249 patients Malignant chondroblastoma presenting
of the bone. Hum Pathol 2010;41(2): examined for a bone tumor. Clin Orthop as a recurrent pelvic tumor with DNA
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Parker SG: Metastatic chondroblastoma: Radiographic and histologic patterns of

April 2013, Vol 21, No 4 233


Review Article

Understanding Systematic
Reviews and Meta-analyses in
Orthopaedics

Abstract
Kelly A. Lefaivre, MD, MSc, The systematic literature review is a powerful tool for summarizing
FRCSC and evaluating current knowledge related to a specific research
Gerard P. Slobogean, MD, MPH, question. Systematic reviews have many advantages over
FRCSC traditional narrative reviews. A meta-analysis of data from a
systematic review can provide a better estimate of a treatment
effect than can individual studies. To ensure quality conclusions,
rigorous methods must be applied to systematic reviews, such as
formulation of a specific research question, systematic literature
search, selection and assessment of included studies, data
extraction, quality assessment of included studies, meta-analysis
and presentation of results, and formation of conclusions. Threats
to the internal validity and generalizability of the conclusions of
systematic reviews include lack of clarity or appropriateness of the
research question, poor quality of the included studies,
heterogeneity of results between studies, inappropriate
conclusions, and inappropriate application in clinical practice.

C linicians now work in the era of


evidence-based medicine. The
focus on evidence from clinical re-
treatment decisions.
A systematic literature review is fo-
cused on a single research question
search has necessitated a new skill that tries to identify, appraise, and
set in the practice of medicine.1,2 The select all relevant literature relevant
From the University of British ability to search the literature and to to that question. When appropriate,
Columbia, Vancouver, BC, Canada. appropriately evaluate clinical re- this is followed by a meta-analysis,
Dr. Lefaivre or an immediate family
search literature is now a core part or synthesis of data extracted from
member has received research or of orthopaedic training.3 relevant studies.5 The systematic re-
institutional support from Synthes. view is a study in itself and, as such,
Trying to keep up-to-date on the
Neither Dr. Slobogean nor any
immediate family member has volume of available medical litera- adheres to strict scientific design
received anything of value from or ture can be daunting, and the litera- based on explicit, prespecified, and
has stock or stock options held in a ture in any given subject area may be reproducible methods. Thus, such a
commercial company or institution review can provide a more reliable
contradictory, confusing, misinter-
related directly or indirectly to the
subject of this article. preted, and/or mispresented.4 In ad- estimate of the answer to the speci-
dition, seemingly similar studies can fied research question than can any
J Am Acad Orthop Surg 2013;21:
present contradictory conclusions as single study. When it is not possible
245-255
a result of biases, differences in to draw such conclusions, the good
http://dx.doi.org/10.5435/ systematic review instead can dem-
JAAOS-21-04-245 methodology or outcome measure,
or chance. In such cases, it can be onstrate where knowledge is lacking
Copyright 2013 by the American
impossible to know which results and thereby direct future research.6,7
Academy of Orthopaedic Surgeons.
should be relied on to make the best The standard for systematic re-

April 2013, Vol 21, No 4 245


Understanding Systematic Reviews and Meta-analyses in Orthopaedics

views and meta-analysis in medicine Table 1


is set by The Cochrane Collabora-
Differences Between Systematic Reviews and Narrative Reviews
tion, which publishes the Cochrane
Database of Systematic Reviews sec- Feature Systematic Review Narrative Review
tion of The Cochrane Library. These Question Focused clinical question Often broad in scope
articles focus on the systematic re- Sources and Comprehensive sources and Not usually specified, potentially
view of randomized controlled stud- search explicit search strategy biased
ies, which follow an eight-step Study selection Criterion-based selection, uni- Not usually specified, potentially
process: defining a question and de- formly applied biased
veloping inclusion criteria, searching Study appraisal Rigorous critical appraisal Variable
for studies, selecting studies and col- Synthesis Quantitative summary that in- Often a qualitative summary
lecting data, assessing risk of bias, cludes statistical synthesis
when possible (meta-
data analysis and meta-analyses, ad- analysis)
dressing biases, presenting results, Inferences Usually evidence-based Sometimes evidence-based
and interpreting results and drawing
conclusions.8 However, randomized Adapted with permission from Cook DJ, Mulrow CD, Haynes RB: Systematic reviews:
Synthesis of best evidence for clinical decisions. Ann Intern Med 1997;126(5):376-380.
controlled studies are rare in ortho-
paedics; thus, the best available evi-
dence may come from observational
studies. The validity and quality of a view often addresses a broad range
systematic review is inherently de- of issues related to a topic. A review Conducting a Systematic
pendent on the quality of included is likely narrative if the specific re- Review of the Literature
studies, and special attention must be search question is not identified in
paid to methodology, qualitative the introduction or if the review Formulating a Research
analysis, and confounding.9 Interpre- lacks a methods section.11 Question
tation of systematic reviews is made By definition, a systematic review The first step in any systematic re-
even more complicated by variability is a scientific investigation in itself, view of the literature is to formulate
in the quality of included studies and with preplanned, reproducible meth- the primary research question that
in the methodology of the systematic ods. The individual studies are the the review seeks to answer. The clas-
review itself. subjects in a properly performed sys- sic systematic review evaluating in-
tematic review, and they are uni- tervention effects has five elements:
formly included or excluded based population, intervention, compara-
Systematic Review Versus on predetermined defined criteria. In tors, outcomes, and study design
Traditional Narrative contrast, in a narrative review, the (PICOS).12 When designing a ques-
Review study sources and selection are rarely tion, the authors should address the
specified and are inherently open to population in question, intervention
Review articles have long had a role bias both in their selection and pre- of interest, a control or alternative
in the interpretation and synthesis of sentation. In systematic reviews, ap- intervention, an outcome measure,
the literature. The difference between praisal of the included studies is rig- and included study designs or level
a well-performed systematic litera- orous, with attention paid to the of evidence13-15 (Table 2). However,
ture review and a traditional narra- methodology and other properties of systematic reviews can be used to an-
tive review hinges on the extent to included studies. This is rarely the swer many more research questions
which the scientific review methods case in narrative reviews. than those related to intervention
were used to minimize error and Systematic reviews are less subject effects16-22 (Table 3).
bias10 (Table 1). to bias and, when performed well, The scope of the question is an im-
The systematic review is designed lead to an evidence-based conclu- portant consideration. If the scope is
to exhaustively answer a specific, of- sion. Narrative reviews are useful in too broad, the amount of literature
ten very narrow, clinical question. describing the history of a problem may be too large or too heteroge-
These questions define the patient and its management, and they may neous to allow for successful comple-
population, condition of interest, in- be useful in describing developments tion of the review. If the scope is too
tervention of interest, and outcome for which research is scant or prelim- narrow, there may be insufficient evi-
measure. In contrast, a narrative re- inary. dence to carry the review. Broad

246 Journal of the American Academy of Orthopaedic Surgeons


Kelly A. Lefaivre, MD, MSc, FRCSC, and Gerard P. Slobogean, MD, MPH, FRCSC

Table 2
Use of the PICOS Format for Systematic Literature Review
Population Intervention Comparator Outcomes Study Design Question

Patients undergo- Single-bundle Double-bundle 1. KT-1000 All comparative Using all comparative study
ing ACL recon- reconstruction reconstruction arthrometer study designs designs, is double-bundle su-
struction (MEDmetric) perior to single-bundle recon-
2. Pivot-shift test- struction when comparing
ing postoperative KT-1000 ar-
thrometer (MEDmetric) and
pivot-shift testing?
Patients undergo- No patellar resur- Patellar resurfac- 1. Frequency of RCTs Based on RCT data, does pa-
ing primary TKA facing ing reoperation tellar resurfacing decrease
2. Postoperative the incidence of reoperations
anterior knee and postoperative anterior
pain knee pain and improve knee
3. Improvement in scores compared with not
knee scores resurfacing the patella during
primary TKA?
Children with dis- Crossed K-wire Lateral-only Iatrogenic ulnar All comparative Using all comparative study
placed supracon- fixation K-wire fixation nerve injury study designs designs, what is the risk of
dylar fractures of iatrogenic ulnar nerve injury
the humerus with crossed K-wire fixation
versus lateral-only K-wire fix-
ation in children with dis-
placed supracondylar fracture
of the humerus?

ACL = anterior cruciate ligament; K-wire = Kirschner wire; PICOS = population, intervention, comparators, outcomes, study design;
RCT = randomized controlled trial; TKA = total knee arthroplasty

questions can be broken down into Table 3


several related, more specific ques-
Types of Research Question Addressed in Systematic Reviews
tions. In such cases, each question
should be treated as an individual Questions From Published
Type of Question Systematic Reviews
systematic review.
Intervention effects (PICOS) What is the difference in clinical results, with re-
Literature Search gard to rates of mortality and revision surgery,
of prosthetic replacement compared with inter-
Prior to searching the literature, the nal fixation in the treatment of femoral neck
specific research question must be in- fractures in patients aged ≥65 years based on
terpreted as a set of strict inclusion RCTs?16
and exclusion criteria. These criteria Sequelae of disease or What are the complications associated with
interventions locked plate fixation of proximal humerus frac-
determine the methodology of paper tures?18
selection following the literature
Frequency of disease or What are the geographic trends of the incidence
search. The inclusion and exclusion condition of osteoporotic hip fractures?19
criteria must address the specific ar- Diagnostic accuracy What is the measurement methodology and in-
eas outlined in the research question. terpretation of radiographic displacement in
Level I studies, or randomized con- studies of pelvic ring fractures in adults?20
trolled trials, are the standard for Disease etiology and/or risk Does delay to surgery in patients aged ≥65
factors years have an effect on mortality and rate of
systematic reviews. However, in or- complications?21
thopaedics, as in many medical
Prognosis What patient and injury factors are prognostic for
fields, the best available evidence return to work and duration of disability follow-
may be level III and IV studies.9,12,23 ing orthopaedic trauma?22
In such cases, it is appropriate to in-
PICOS = population, intervention, comparators, outcomes, study design; RCT = randomized
clude lower level studies in the inclu- controlled trial
sion and exclusion criteria; however,

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Understanding Systematic Reviews and Meta-analyses in Orthopaedics

Table 4 Because the literature search itself is


a key part of the methods in a system-
MEDLINE and Embase Search Strategy on the Topic of
Thromboprophylaxis for Pelvic and Acetabular Fractures atic review, the search strategy should
be published either in the article or as
MEDLINE Embase
an appendix, including the date the
Pulmonary embolism/ Exp thromboembolism/ search was performed. As with any sci-
Thrombosis/ Pulmonary embolism.tw entific publication, the methods of a
Thromboembolism/ Thrombosis.tw systematic review should be repeatable,
Venous thrombosis/ Thromboembolism.tw and this is possible only when they are
Pulmonary embolism.tw Venous thrombosis.tw clearly stated.
Thrombosis.tw Deep vein thrombosis.tw
Thromboembolism.tw Pelvi$ fracture.tw Selection and Assessment
Venous thrombosis.tw Acetabul$ fracture.tw Methods
Deep vein thrombosis.tw Acetabulum/ Transparency and repeatability are
Exp pelvic bones/ Exp pelvic girdle
just as important in study selection
Pelvi$ fracture.tw Pelvis fracture/
as in the methodology. In a well-
Acetabul$ fracture.tw or/1-6
performed systematic review, the
or/1-9 or/7-11
“who” and “how” of every stage of
or/10-12 Combine
the selection should be clearly stated.
Combine
To minimize bias and decrease the
Adapted with permission from Slobogean GP, Lefaivre KA, Nicolaou S, O’Brien PJ: A likelihood that papers are missed,
systematic review of thromboprophylaxis for pelvic and acetabular fractures. J Orthop two independent observers should
Trauma 2009;23(5):379-384.
perform each stage of the selection.29
Typically, the search returns a large
doing so will affect the strength of plements for additional informa- number of titles collected. These
the conclusions. A well-performed tion.26 should be combined and duplicates
systematic review of low-level litera- The formation of a search strategy removed. This list represents the list
ture often serves as a thorough de- is driven by the design of the two da- of titles to be searched by the two in-
scription of the state of the literature tabases, which are unique. It is im- dependent observers. The titles se-
around a specific question and func- portant to cast a net that is wide lected by the observers are com-
tions to direct future research rather enough to capture all possible arti- bined, duplicates are removed, and
than to provide strong answers to cles, but not so wide that the author any title selected by either reviewer is
clinical questions or to serve as the must search through, for example, included in the abstract review. The
basis for practice guidelines. 5,000 titles. The assistance of a med- same process is repeated for the ab-
The publication type and status ical librarian with expertise in these stracts. Next, the full manuscripts
must be determined at this stage, as databases can be invaluable at the are reviewed for suitability based on
well, because a proper systematic re- outset. An example of a search strat- inclusion and exclusion criteria, and
view requires the use of more re- egy from a recent systematic review final selections are made. Often, it is
sources than PubMed alone. The of deep vein thrombosis prophylaxis best to include resources found in
MEDLINE (PubMed) and Embase in pelvic fracture patients is shown in bibliographic reviews or recent meet-
bibliographic databases each house Table 4.27 Additional searching is re- ings in the final manuscript review
millions of references, which has quired to minimize bias, including stage and the abstract stage, respec-
made literature searches much eas- searching reference lists from rele- tively.12
ier.24,25 The overlap between these da- vant studies and searching by hand Documentation and presentation
tabases varies by subject area but is both conference proceedings and re- of the study selection process are
at most 66%; thus, both must be cent issues of key journals. If the key. A flowchart showing the num-
searched.22 In orthopaedics specifi- manual reference search turns up ber of studies selected and excluded
cally, the use of these two databases many articles that the database at each stage is a clear way to docu-
alone has been shown to be suffi- search missed, the original search ment this. The authors also should
cient, with the addition of a search strategy should be reviewed and provide additional detail with regard
of conference proceedings and sup- broadened, if necessary.28 to studies that were excluded at the

248 Journal of the American Academy of Orthopaedic Surgeons


Kelly A. Lefaivre, MD, MSc, FRCSC, and Gerard P. Slobogean, MD, MPH, FRCSC

Figure 1

Hypothetical flow diagram of the study selection process for systematic literature reviews, with associated research
steps.

final stage and the reason for their Data extraction typically includes geneity in the measurement of out-
exclusion (Figure 1). general information about the arti- comes poses a significant challenge
cle, study characteristics, participant in the pooling of results of treatment.
Data Extraction characteristics, intervention, and The method of measuring outcomes
The fourth stage in every systematic outcome data. Outcome data are of- in orthopaedics has itself been the
review consists of data extraction ten the most complicated to extract topic of many systematic reviews.20,30
from the selected studies. The exact because attention needs to be paid
data points extracted should be not only to the outcome itself but Quality Assessment
clearly stated in the methods section also to how it was measured and Before attempting any synthesis of
and should be easy for the reader to how the measurement was standard- data, the authors must consider and
follow through to the results section. ized. In orthopaedic studies, hetero- report on the study quality. In broad

April 2013, Vol 21, No 4 249


Understanding Systematic Reviews and Meta-analyses in Orthopaedics

terms, a quality assessment answers Meta-analysis and of differences in study populations, in-
the question of how close to the Presentation of Results terventions, outcome measurement, or
“truth” are a study’s findings or con- study methodology. The Q, H, and I2
The systematic, reproducible sum-
clusions.12,28 It is important to detect are some of the statistical tests that
mary and presentation of studies an-
significant sources of bias because have been described to quantify het-
swering a specific research question
these can have as much influence on erogeneity in this setting. The I2 sta-
is in itself a systematic review (ie,
the outcome as any other factor. tistic is the easiest to interpret and
qualitative systematic review). In
Historically, quality assessment has the most commonly used in health-
consisted of the application of a list some cases, the review process is care meta-analyses. It provides a pro-
of criteria, such as those published in stopped and the findings presented at portion of the between-study vari-
the Cochrane Handbook for System- this stage because of study heteroge- ability in the intervention effect that
atic Reviews of Interventions, to neity, lack of appropriate studies, or is attributable to study heterogeneity,
evaluate the methodology of ran- other reasons. The combination of or how much of the variability is not
domized controlled trials.8 These cri- results from such studies is known as due to chance. It is generally ac-
teria include randomization and a meta-analysis (ie, quantitative sys- cepted that ≤25% is indicative of lit-
blinding, as well as evaluation for tematic review). tle heterogeneity, 50% shows moder-
confounders, study dropouts, and A meta-analysis is a statistical ate heterogeneity, and 75% is
intention-to-treat analysis. combination of results from two or indicative of a high degree of hetero-
Evaluation of bias in systematic re- more similar studies. This is not a geneity.33
views of observational, or lower- simple arithmetic combination of re- Results from systematic reviews
quality, studies is even more complex. sults; rather, it is a weighted average and meta-analyses typically have two
In these cases, the authors must con- that gives proportional weight to the key elements: a table of included
sider the appropriateness of the study number of subjects in each study. study characteristics and forest plots.
design, the sources of bias, choice of Further, the statistical methods of The table is a simple representation
outcome measure, statistical issues, meta-analysis take into account of the studies selected for inclusion
quality of reporting, intervention, and intra- and interstudy variability and typically identifies the author,
generalizability of the results.9 Sev- when combining the results. year of publication, source journal,
eral scales have been devised to rate The two types of model that are and other information relevant to the
the quality of observational studies. commonly used to statistically com- specifics of the systematic review.
The Newcastle-Ottawa Scale uses a bine results are the fixed effects The forest plot is a graphic represen-
star system in which each study is model and the random effects model. tation of the meta-analysis, with a
judged on three broad categories: se- The first assumes a constant treat- representation of the statistical
lection of the study groups, compa- ment effect between studies, whereas weight of each study as well as the
rability of the groups, and ascertain- the second assumes that the effect is CIs. An example of a forest plot is
ment of either the exposure or randomly distributed between the seen in Figure 2.34
outcome of interest for case-control studies. In short, the fixed effects Regression may be appropriate in
or cohort studies, respectively.31 model assumes that the study itself is meta-analyses in which other impor-
The findings of the quality assess- the only variable, whereas the ran- tant reported variables may have an
ment can be used by authors in sev- dom effects model introduces a sec- effect on the treatment effect. Meta-
eral ways. First, a narrative synthesis ond source of variation between regression is used in meta-analyses
of quality can be performed to ex- studies. Typically, the random effects to evaluate the effect of moderator
plain differences across results in model produces more conservative variables on a study effect using
studies included in the systematic re- estimates, indicated by wider confi- regression-based techniques (ie, esti-
view. Conversely, for a systematic re- dence intervals (CIs).32 mating the effect of the moderator
view that is carried on to a meta- Evaluation of study heterogeneity is variable while controlling for other
analysis, the findings can be another key element of the statistical variables in the model). Fixed-effect
incorporated into the data synthesis testing needed for a meta-analysis. In meta-regression does not allow for
using subgroup or sensitivity analy- this context, heterogeneity refers to the the specification of within- and
ses. Regardless of approach, study amount of variability between the re- between-study variation. Instead, the
quality should be clearly addressed sults of individual studies compared authors can use random-effects
in some way by the authors of a with what would be expected by meta-regression, accounting for
well-performed systematic review.12,32 chance. Variability could be the result between-study variation.35

250 Journal of the American Academy of Orthopaedic Surgeons


Kelly A. Lefaivre, MD, MSc, FRCSC, and Gerard P. Slobogean, MD, MPH, FRCSC

Figure 2

Example of a forest plot of simple decompression versus transposition of the ulnar nerve for cubital tunnel syndrome.
The references cited in this figure do not appear in this article, and the data have not been verified for accuracy: Biggs
et al, Neurosurg, 2006; Bartels et al, Neurosurg, 2005; Taha et al, Neurosurg, 2004; Bimmler et al, Ann Hand Surgery,
1996; Davies et al, Aust NZ J Surg, 1991; Adelaar et al, J Hand Surg Am, 1984; Foster et al, J Hand Surg, 1981;
Chan et al, Neurosurg, 1980; MacNicol et al, J Bone Joint Surg Br, 1979; Paine et al, Can J Surg, 1970.
CI = confidence interval. (Reproduced with permission from Macadam SA, Gandhi R, Bezuhly M, Lefaivre KA: Simple
decompression versus anterior subcutaneous and submuscular transposition of the ulnar nerve for cubital tunnel
syndrome: A meta-analysis. J Hand Surg Am 2008;33[8]:1314.e1-12.)

Making recommendations or conclusions, and inappropriate ap-


drawing conclusions after perform- Pitfalls of Systematic plication in clinical practice.
ing a systematic review and meta- Reviews and The primary weakness of system-
analysis requires a clear assessment Meta-analyses atic review methodology is the retro-
of the strength of the recommenda- spective collection of data that has
Summarizing the results of primary
tions, based on the quality of the in- been published by other authors. Re-
literature using scientific methodol-
cluded trials. The GRADE (Grading lying on the work of previous au-
ogy is the characteristic strength of a
of Recommendations Assessment, thors leads to the potential criticism
Development, and Evaluation) work- systematic review. A well-conducted of “garbage in, garbage out.” The
ing group, started in 2000, offers a systematic review is an important strength of the systematic review is
system for rating the quality of evi- evidence-based medicine tool that directly related to the strength of the
dence in systematic reviews and provides qualitative and quantitative available literature. The use of
guidelines and for grading the summaries when individual studies poorly designed and underpowered
strength of recommendations in cannot offer definitive conclusions. studies as the basis of a systematic
guidelines.36 A series of articles that Although systematic reviews are im- review results in limited and poten-
were recently published in the Jour- portant tools, the power of summa- tially flawed conclusions.
nal of Clinical Epidemiology outlines rizing multiple studies can be equally Outlining a specific clinical ques-
the most current application and in- problematic. Pitfalls of systematic re- tion and applying strict eligibility cri-
terpretation of the GRADE guide- views and meta-analyses include im- teria for included studies can prevent
lines.37 proper statistical pooling, misleading many problems. McKee et al38 re-

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Understanding Systematic Reviews and Meta-analyses in Orthopaedics

cently published a meta-analysis that for between-study heterogeneity is an are generalizable to his or her clinical
followed these basic principles to en- important final step to determine scenario. This includes ensuring sim-
sure its validity and clinical useful- whether and how the results of mul- ilar patient populations, interven-
ness. In their review, they sought to tiple studies should be pooled. tions, and outcomes of interest. Con-
compare the outcomes of surgical These principles of data analysis sider the following clinical scenario.
versus nonsurgical care for displaced and methodology were applied to the A 14-year-old elite hockey player
midshaft clavicle fractures. A search meta-analysis of 16 observational presents with an acute midshaft clav-
for studies related to clavicle fracture studies in a systematic review of the icle fracture. The injury occurred
management would identify several effect of early surgery on hip fracture during the off-season, and it is com-
hundred articles; however, by defin- mortality.21 The methodologic qual- pletely displaced, with 2 cm of short-
ing their research question, the sys- ity of each included study was as- ening. The patient and family want
tematic review was limited to the sessed using the Newcastle-Ottawa to know whether surgical treatment
handful of relevant articles that com- Scale, and the authors tested clini- is the best option to restore shoulder
pare these two treatments in the cally plausible factors that could ex- function for the upcoming season.
specified midshaft fracture pattern. plain heterogeneity between studies. You counsel the family that the re-
Furthermore, to minimize the poten- More importantly, they recognized cent meta-analysis of randomized
tial of pooling studies with poor in- that differences in mortality between controlled trials by McKee et al38
ternal validity (ie, methodologic early and late treatment groups demonstrates better functional out-
flaws), the authors chose to include might have been due to confounding comes (weighted Constant score 94.3
only randomized controlled trials factors present in the observational versus 90.2) and lower nonunion
that compared surgical and nonsur- study designs. For example, sicker rates (RR 0.18; 95% CI, 0.06 to
gical treatments. Finally, the defined patients often require more preoper- 0.51) with surgical fixation than
outcomes of interest—patient func- ative evaluations than their healthier nonsurgical treatment. Is this advice
tion and treatment complications— counterparts. As a result, the authors appropriate?
ensured a balanced reporting of evi- performed stratified analyses, with A closer look at the trials included
dence that would not inadvertently one analysis pooling all included in the meta-analysis by McKee et al38
focus on the positive or negative studies and a second consisting of a shows that the clinical scenario and
characteristics of a given treatment. meta-analysis of the five studies that the meta-analysis populations are
Even when the methodology is cor- had been statistically adjusted for different. The mean patient age
rectly designed, several pitfalls re- age, sex, and comorbidities. Finally, among the included studies ranged
main in the data analysis stage. Even the authors provided additional from 25 to 41.3 years. Furthermore,
in a review that includes only ran- analyses of mortality at 30 days, 6 the current trial literature may not
domized controlled trials, method- months, and 1 year to improve the apply to adolescents because of the
ologic weakness within the included relevance of the results. This proved potential in children for correction of
studies can significantly influence the to be important to understanding the malalignment and shortening via late
conclusions of the review. As a re- treatment effects because, although closure of the clavicular physes.39
sult, the authors and readers must in- the benefits of early surgery are not Surgical fixation ultimately may be
terpret the results of any pooled significant at 30 days (relative risk the optimal treatment in the clinical
analysis in the context of the quality [RR] 0.90; 95% CI, 0.71 to 1.13), scenario presented; however, it is im-
of each individual study. Some au- substantial risk reduction is demon- portant to recognize that it is easy to
thors may choose to exclude low- strated at 1 year (RR 0.55; 95% CI, inappropriately apply the results of a
quality studies or to perform sensi- 0.40 to 0.75). This example demon- systematic review because important
tivity analyses to determine the strates that the conclusions of a methodologic details from each in-
influence of these studies on the meta-analysis can be misleading if cluded study may be omitted from
pooled results. In the data analysis clinically relevant stratification and the meta-analysis manuscript.
phase, it is important to ensure that contextualization are not performed.
the included studies are appropriate The final difficulty in using system-
to pool based on clinically similar atic review or meta-analysis data lies Critically Evaluating
patient populations, confounding in applying the results to clinical Systematic Reviews
factors, and other differences be- practice. The reader must critically
tween studies that may have influ- determine whether the individual Critical appraisal of a systematic re-
enced the results. Statistical testing studies pooled in the meta-analysis view or meta-analysis requires a

252 Journal of the American Academy of Orthopaedic Surgeons


Kelly A. Lefaivre, MD, MSc, FRCSC, and Gerard P. Slobogean, MD, MPH, FRCSC

Table 5 porting in meta-analyses was ad-


dressed by an international group
Six Key Appraisal Questions for a Systematic Review According to the
Centre for Evidence-based Medicine42 that developed the QUOROM (qual-
ity of reporting of meta-analyses)
Are all elements of the research question clearly stated (ie, PICO)?
statement. In 2009, this guideline
Are all relevant studies identified?
was updated to address advances in
Are the inclusion criteria appropriate?
the science of systematic reviews,
Are the included studies sufficiently valid to answer the research question?
and it was renamed PRISMA (pre-
Are the results between studies similar?
ferred reporting items for systematic
Are the results appropriately presented?
reviews and meta-analyses).41 This
PICO = population, intervention, comparators, outcome of interest guideline is a 27-point checklist that
can be used by authors and evalua-
tors of systematic reviews and meta-
stepwise approach to assessing the search has not been identified. This analyses to ensure that maximum
methodology and conclusions pre- may include manuscripts in lan- quality is achieved.
sented by the authors. The applica- guages other than English, unpub- Critical appraisal of a systematic
tion and interpretability of assess- lished data, or literature that has review or meta-analysis requires a
ment tools can be challenging, been published since the initial stepwise evaluation to ensure that
particularly for surgical interven- search. Once the reader is satisfied the review can answer the reader’s
tions.40,41 In general, the clinician that the search strategy is compre- clinical question and that the results
must evaluate the ability of the re- hensive, she or he must ensure that of the review provide a transparent
view to define the research question the review clearly outlines the meth- and valid summary of the relevant
(ie, population, intervention, com- odology used for selecting the in- literature.
parison, outcome of interest), search cluded studies. This includes adher-
strategy, pooling methods, and con- ing to a priori eligibility criteria and
clusions. the use of a systematic approach in Summary
The Centre for Evidence-based reviewing potential studies. In addi-
Medicine (CEBM) developed a sim- tion, the reader must consider how Systematic reviews and meta-
ple appraisal checklist, which is the choice of eligible study designs analyses are powerful tools with
available online.42 The CEBM Sys- affects the pooled results. For exam- which to make evidence-based con-
tematic Review Appraisal Sheet out- ple, are observational studies pooled clusions where single studies fall
lines six important aspects of the re- with randomized trial data? Combin- short. The essential steps in a well-
view to be appraised and clearly ing the results of less powerful study performed systematic review are the
defines what information should be designs increases the propensity for formulation of an appropriate and
present in a valid review and where bias. specific research question, a system-
in the manuscript the information Similar issues of validity must be atic literature search, transparent se-
should be reported (Table 5). considered when appraising the lection and assessment of included
Other questions should be consid- methods of statistical pooling. Were studies, data extraction, quality as-
ered, as well, when interpreting the the included studies appropriate for sessment of included studies, quanti-
results of a systematic review.43 For pooling? Were tests of heterogeneity tative systematic review or meta-
example, the objective and inclusion performed? In the presence of het- analysis of results, and formation of
criteria must match the clinical ques- erogeneity, is there a plausible expla- conclusions.
tion for which an answer is being nation for it? Were appropriate As with all types of scientific re-
sought. Once this is confirmed, more methods used for combining the re- search, there are many potential
attention to the details of the meth- sults? These questions must be threats to the internal validity and
odology is warranted. answered to ensure that the pooled generalizability of the conclusions of
The search strategy must be com- results can be appropriately inter- systematic reviews. Critical evalua-
prehensive and should attempt to preted. Finally, the reader must take tion of systematic reviews requires
identify studies beyond the initial care to ensure that the conclusions that special attention be paid to the
bibliographic database search re- made by the authors are supported clarity and appropriateness of the re-
sults. The reader must decide how by the results presented. search question, the methodology of
likely it is that additional relevant re- The issue of suboptimal quality re- study identification and inclusion,

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Understanding Systematic Reviews and Meta-analyses in Orthopaedics

the quality of the included studies, studies in orthopaedic research. J Bone acute orthopaedic trauma. Injury 2010;
Joint Surg Am 2009;91(suppl 3):87-94. 41(8):787-803.
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views reach uncertain conclusions. BMJ Osteoporos Int 2011;22(10):2575-2586. ca/programs/clinical_epidemiology/
2003;326(7392):756-758. oxford.asp. Accessed January 17, 2013.
20. Lefaivre KA, Slobogean G, Starr AJ, Guy
7. Brown P, Brunnhuber K, Chalkidou K, P, O’Brien PJ, Macadam SA: Methodol- 32. Egger M, Davey Smith G, Altman D:
et al: How to formulate research recom- ogy and interpretation of radiographic Systematic Reviews in Health Care:
mendations. BMJ 2006;333(7572):804- outcomes in surgically treated pelvic Meta-Analysis in Context. London,
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Trauma 2012;26(8):474-481. Group, 2001, pp 122-210.
8. Higgins JP, Green S, eds: Cochrane
Handbook for Systematic Reviews of 21. Simunovic N, Devereaux PJ, Sprague S, 33. Higgins JP, Thompson SG: Quantifying
Interventions, version 5.1.0 (updated et al: Effect of early surgery after hip heterogeneity in a meta-analysis. Stat
March 2011). Oxfordshire, United King- fracture on mortality and complications: Med 2002;21(11):1539-1558.
dom, The Cochrane Collaboration, Systematic review and meta-analysis.
2011. CMAJ 2010;182(15):1609-1616. 34. Macadam SA, Gandhi R, Bezuhly M,
Lefaivre KA: Simple decompression ver-
9. Simunovic N, Sprague S, Bhandari M: 22. Clay FJ, Newstead SV, McClure RJ: A sus anterior subcutaneous and submus-
Methodological issues in systematic re- systematic review of early prognostic cular transposition of the ulnar nerve for
views and meta-analyses of observational factors for return to work following cubital tunnel syndrome: A meta-

254 Journal of the American Academy of Orthopaedic Surgeons


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analysis. J Hand Surg Am 2008;33(8): 38. McKee RC, Whelan DB, Schemitsch EH, JAMA 2000;283(15):2008-2012.
1314.e1-12. McKee MD: Operative versus nonopera-
tive care of displaced midshaft clavicular 41. Moher D, Liberati A, Tetzlaff J, Altman
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39. Smekal V, Oberladstaetter J, Struve P,
36. GRADE working group website. http:// Krappinger D: Shaft fractures of the 42. Centre for Evidence-based Medicine
www.gradeworkinggroup.org. Accessed clavicle: Current concepts. Arch Orthop (CEBM): Critical appraisal. Available at:
January 17, 2013. Trauma Surg 2009;129(6):807-815. http://www.cebm.net/index.aspx?o=
1157. Accessed January 17, 2013.
37. Guyatt GH, Oxman AD, Schünemann 40. Stroup DF, Berlin JA, Morton SC, et al:
HJ, Tugwell P, Knottnerus A: GRADE Meta-analysis of observational studies in 43. Yuan Y, Hunt RH: Systematic reviews:
guidelines: A new series of articles in the epidemiology: A proposal for reporting. The good, the bad, and the ugly. Am J
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Epidemiol 2011;64(4):380-382. in Epidemiology (MOOSE) group.

April 2013, Vol 21, No 4 255


On the Horizon From the ORS
Annexins: Novel Therapeutic Targets for
the Treatment of Osteoarthritis?
Takeshi Minashima, PhD Osteoarthritis (OA) is the most (ADAMTS)-5, inducible nitric ox-
Kirk Campbell, MD common form of arthritis, affecting ide synthase (iNOS), interleukin
an estimated 27 million Ameri- (IL)-6, and matrix metalloprotein-
Thorsten Kirsch, PhD cans.1 The lack of current treat- ase (MMP)-13, in IL-1–treated
ments to slow OA progression is mouse articular chondrocytes,
due to the lack of both early detec- whereas overexpression of AnxA6
tion methods and therapeutic tar- resulted in increased NF-κB activity
gets for OA. Thus, there is an ur- and mRNA levels of these catabolic
gent need for the discovery of markers in articular chondrocytes.
potential new therapeutic targets Cartilage destruction in IL-1–
for the treatment of OA. treated knee joints of AnxA6
Annexins are cytoplasmic pro- knockout mice was markedly re-
teins that, in the presence of Ca2+, duced compared with cartilage de-
translocate and bind to mem- struction in wild-type mouse joints.
branes. The role of annexins in dis- AnxA6 interaction with p65 re-
ease pathology is an emerging field sulted in increased nuclear translo-
of investigation, with many studies cation and retention of the active
highlighting the role of annexins p50/p65 NF-κB complex.
not only as prognostic and diagnos- Based on the detrimental effects
tic markers but also as being ac- of NF-κB signaling on cartilage de-
tively involved in causing diseases struction during OA pathogenesis,
such as Alzheimer’s disease, auto- NF-κB signaling has become a ma-
immunity, cancer, diabetes, and car- jor therapeutic target in OA dis-
diovascular diseases. Specifically, ease.4 Because NF-κB, however,
Topics from the frontiers of basic their modulatory action on major plays a pivotal role in many physio-
research presented by the
Orthopaedic Research Society.
signaling pathways involved in dis- logic processes, selective targeting
ease pathologies has made the an- of this signaling pathway in OA
From the Musculoskeletal Research
nexins novel and exciting therapeu- joints has become a major chal-
Center, Department of Orthopaedic
Surgery, New York University School tic targets.2 lenge. Annexins appear to specifi-
of Medicine, Hospital for Joint We have shown that annexin A6 cally stimulate NF-κB signaling
Diseases, New York, NY. (AnxA6) is highly expressed in OA only during disease pathology but
Dr. Kirsch or an immediate family cartilage but not in normal healthy not under physiologic conditions.
member serves as a paid consultant articular cartilage.3 Because annex- For example, only the high expres-
to Asubio Pharmaceuticals. Neither
ins have been shown to stimulate sion of AnxA1 in breast cancer cells
of the following authors nor any
immediate family member has nuclear factor kappa B (NF-κB) sig- results in constitutive activation of
received anything of value from or naling, a major catabolic signaling NF-κB and ultimately high metas-
has stock or stock options held in a pathway in OA,4-6 we tested the tasis of these cancer cells, whereas
commercial company or institution
related directly or indirectly to the
possibility that AnxA6 stimulates low expression of AnxA1 does not
subject of this article: Dr. Minashima NF-κB signaling in OA cartilage, lead to constitutive NF-κB activa-
and Dr. Campbell. thereby leading to accelerated carti- tion and, as a consequence, low
J Am Acad Orthop Surg 2013;21: lage destruction. Loss of AnxA6 re- metastasis.5 Similarly, our findings
256-257 sulted in decreased activation of suggest that only high expression of
http://dx.doi.org/10.5435/ NF-κB and mRNA levels of cata- AnxA6 in OA cartilage results in
JAAOS-21-04-256 bolic markers, including a dis- NF-κB activation, whereas low
Copyright 2013 by the American integrin and metalloproteinase AnxA6 expression in healthy artic-
Academy of Orthopaedic Surgeons. with thrombospondin motif ular cartilage does not. Therefore,

256 Journal of the American Academy of Orthopaedic Surgeons


On the Horizon From the ORS

targeting the modulatory actions of NF-κB activity by annexins require Expression of early and late
differentiation markers (proliferating cell
annexins on NF-κB signaling may their ability to bind Ca2+. Therefore, nuclear antigen, syndecan-3, annexin VI,
provide a novel and selective way to interfering with the Ca2+-binding and alkaline phosphatase) by human
inhibit NF-κB signaling in diseases, ability of these annexins may emerge osteoarthritic chondrocytes. Am J Pathol
2001;159(5):1777-1783.
such as cancer and OA. as a potential novel strategy to spe-
Future research needs to determine cifically inhibit NF-κB activity in OA 4. Marcu KB, Otero M, Olivotto E, Borzi
RM, Goldring MB: NF-kappaB
strategies of how to interfere with and other diseases. signaling: Multiple angles to target OA.
the modulatory role of annexins on Curr Drug Targets 2010;11(5):599-613.
NF-κB signaling. Recent findings 5. Bist P, Leow SC, Phua QH, et al:
showing that AnxA4 modulates References Annexin-1 interacts with NEMO and
NF-κB signaling by directly interact- RIP1 to constitutively activate IKK
complex and NF-κB: Implication in
ing with the p50 unit of the heterodi- 1. Buckwalter JA, Saltzman C, Brown T: breast cancer metastasis. Oncogene
meric p50/p65 NF-κB complex in a The impact of osteoarthritis:
2011;30(28):3174-3185.
Implications for research. Clin Orthop
Ca2+-dependent manner6 suggest Relat Res 2004;(427 suppl):S6-S15. 6. Jeon YJ, Kim DH, Jung H, et al:
that the interactions of annexins 2. Fatimathas L, Moss SE: Annexins as
Annexin A4 interacts with the NF-
with NF-κB signaling components disease modifiers. Histol Histopathol kappaB p50 subunit and modulates NF-
2010;25(4):527-532. kappaB transcriptional activity in a
and, ultimately, the stimulation of Ca2+-dependent manner. Cell Mol Life
3. Pfander D, Swoboda B, Kirsch T: Sci 2010;67(13):2271-2281.

April 2013, Vol 21, No 4 257


On the Horizon From the ORS
Synovial Stem Cells in Musculoskeletal
Regeneration
Kivanc Atesok, MD, MSc The synovium is a thin layer of tor) and can express uridine
M. Nedim Doral, MD connective tissue that lines the joint diphosphoglucose dehydrogenase,
surface, tendon sheaths, and bursae which is a vital enzyme involved in
Onur Bilge, MD at freely moving articulations in the hyaluronan synthesis.3 In vitro
Ichiro Sekiya, MD, PhD body. Embryologic origin of the sy- studies have shown that synovial-
novial tissue is the mesenchymal MSCs have superior potential to
layer, which also gives rise to bone, differentiate into chondrocytes and
cartilage, ligament, and muscle tis- to produce cartilage compared with
Topics from the frontiers of basic sue. The synovium has several MSCs of other origins.4 Moreover,
research presented by the
functions, including lubrication of synovial-MSCs have greater prolif-
Orthopaedic Research Society.
the articulating surfaces, nutrition eration and colony-forming capac-
From the Institute of Medical ity than do other stem cell sources.4
of articular cartilage, and regula-
Science, University of Toronto,
Toronto, Ontario, Canada tion of immune response within the
(Dr. Atesok), the Department of joint. Synovial-MSCs and
Orthopaedics and Traumatology, Cartilage Regeneration
Hacettepe University Medical
School, Ankara, Turkey (Dr. Doral), Synovial Cells Based on the promising results from
the Department of Orthopaedics and The synovium contains two main cell in vitro studies, investigators have
Traumatology, N.E. University
types: type A and type B synoviocytes. launched animal model studies to
Meram Faculty of Medicine, Konya,
Turkey (Dr. Bilge), and the Type A synoviocytes are tissue mac- evaluate the effects of synovial-MSCs
Department of Cartilage rophages and have phagocytic func- in vivo. In a rabbit model with full-
Regeneration, Tokyo Medical and thickness articular cartilage defect,
tions. Type B synoviocytes are
Dental University, Tokyo, Japan
(Dr. Sekiya). fibroblast-like cells and function in Koga et al5 demonstrated that local
the formation of synovial fluid.1 In transplantation of synovial-MSCs re-
Dr. Atesok or an immediate family
member serves as a board member, 2001, De Bari et al2 isolated mesen- sults in extensive cartilage matrix for-
owner, officer, or committee member chymal stem cells (MSCs) from the mation at the defect site. These au-
of the International Society of synovium (Figure 1). Type A sy- thors also observed that in the deeper
Arthroscopy, Knee Surgery, and
noviocytes can be characterized zone of the defect, synovial-MSCs dif-
Orthopaedic Sports Medicine and
the Orthopaedic Research Society. and eliminated from mixed syno- ferentiated into bone cells, whereas
Dr. Doral or an immediate family vial cell populations through a se- synovial-MSCs at the superficial
member serves as a board member, lective culturing process. However, zones differentiated into chondro-
owner, officer, or committee member
of the International Society of type B synoviocytes and synovial- cytes. This observation supported the
Arthroscopy, Knee Surgery, and MSCs have similar phenotypic fea- multilineage differentiation potential
Orthopaedic Sports Medicine. tures, and specific characteristics to of synovial-MSCs according to local
Neither of the following authors nor
clearly differentiate these two cell microenvironments in vivo. In a pig
any immediate family member has
received anything of value from or types from each other have not model, transplantation of synovial-
has stock or stock options held in a been determined yet.1 MSCs into a full-thickness articular
commercial company or institution In terms of immune phenotype, cartilage defect promoted cartilage re-
related directly or indirectly to the
subject of this article: Dr. Bilge and
there are many similarities between generation based on arthroscopic,
Dr. Sekiya. synovial-MSCs and MSCs of other MRI, and histologic analysis as early
J Am Acad Orthop Surg 2013;21:
origins. Both cell types are positive as 3 months after the procedure.6
258-259 for surface markers such as CD44, Bilge et al7 used a rabbit knee
CD90, and CD105. However, cells model as an in vivo culture medium
http://dx.doi.org/10.5435/
JAAOS-21-04-258 derived from synovium, including to evaluate the effects of synovium
synovial-MSCs, have higher expres- on chondrocyte growth. These au-
Copyright 2013 by the American
Academy of Orthopaedic Surgeons. sion of CD44 (a hyaluronan recep- thors observed that cartilage grafts

258 Journal of the American Academy of Orthopaedic Surgeons


On the Horizon From the ORS

Figure 1 bone, tendon, and muscle regenera- eta T: Comparison of human stem cells
derived from various mesenchymal
tion. In a rabbit bone defect model, tissues: Superiority of synovium as a cell
Matsusaki et al12 demonstrated that source. Arthritis Rheum 2005;52(8):
using tissue-engineered construct de- 2521-2529.
rived from synovial-MSCs with hy- 5. Koga H, Muneta T, Ju YJ, et al: Synovial
droxyapatite accelerates osteoinduc- stem cells are regionally specified
according to local microenvironments
tion. In a rat Achilles tendon graft after implantation for cartilage regenera-
model, synovial-MSC implantation tion. Stem Cells 2007;25(3):689-696.
into bone tunnel accelerated early re- 6. Nakamura T, Sekiya I, Muneta T, et al:
modeling of tendon-to-bone heal- Arthroscopic, histological and MRI
ing.13 Another rat model study analyses of cartilage repair after a
minimally invasive method of
showed that synovial-MSCs have transplantation of allogeneic synovial
myogenic potential and contribute to mesenchymal stromal cells into cartilage
Histologic appearance of human defects in pigs. Cytotherapy 2012;14(3):
skeletal muscle regeneration in
synovial mesenchymal stem cells 327-338.
under the phase contrast vivo.14 In spite of these reports, there
microscope 14 days after initial is not sufficient evidence regarding 7. Bilge O, Doral MN, Atesok K, et al: The
effects of the synovium on chondrocyte
plating. osteogenic and myogenic potential of growth: An experimental study. Knee
synovial-MSCs compared with bone Surg Sports Traumatol Arthrosc 2011;
19(7):1214-1223.
that are in direct contact with the sy- marrow– and muscle-derived MSCs.
8. Horie M, Driscoll MD, Sampson HW,
novium produce more chondrocytes et al: Implantation of allogenic synovial
compared with cartilage grafts that Future Perspectives stem cells promotes meniscal
regeneration in a rabbit meniscal defect
are not. Studies of animal meniscal In vitro and animal model studies model. J Bone Joint Surg Am 2012;
defect models demonstrated that support the use of synovial-MSCs in 94(8):701-712.
transplanted synovial-MSCs adhere cartilage regeneration as an impor- 9. Horie M, Sekiya I, Muneta T, et al:
to sites of meniscal injury, differenti- tant, arguably superior, cell-based Intra-articular injected synovial stem
cells differentiate into meniscal cells
ate into cells resembling meniscal fi- treatment alternative. Further inves- directly and promote meniscal
brochondrocytes, and enhance me- tigations in the near future should regeneration without mobilization to
distant organs in rat massive meniscal
niscal regeneration.8,9 help in our understanding the com-
defect. Stem Cells 2009;27(4):878-887.
Sporadic human studies have re- plexity of synovial-MSC biology in
10. Morito T, Muneta T, Hara K, et al:
ported that the number of synovial- terms of isolation, characterization, Synovial fluid-derived mesenchymal stem
MSCs in synovial fluid increases in culturing, distinguishing from, and cells increase after intra-articular
knees with degenerated cartilage and interacting with other cell types be- ligament injury in humans.
Rheumatology (Oxford) 2008;47(8):
osteoarthritis and following intra- fore this promising cell-based ther- 1137-1143.
articular ligament injury.10,11 This ob- apy can be translated into clinical 11. Sekiya I, Ojima M, Suzuki S, et al:
servation raises the question whether practice. Human mesenchymal stem cells in
the number of synovial-MSCs that synovial fluid increase in the knee with
degenerated cartilage and osteoarthritis.
are mobilized from synovium into J Orthop Res 2012;30(6):943-949.
synovial fluid increases according to References
12. Matsusaki M, Kadowaki K, Tateishi K,
the degree of cartilage degeneration et al: Scaffold-free tissue-engineered
as part of the reparative process. Hu- 1. Fox DB, Warnock JJ: Cell-based construct-hydroxyapatite composites
meniscal tissue engineering: A case for generated by an alternate soaking
man trials investigating the effects of synoviocytes. Clin Orthop Relat Res process: Potential for repair of bone
intra-articular synovial-MSC trans- 2011;469(10):2806-2816. defects. Tissue Eng Part A 2009;15(1):
55-63.
plantation to promote cartilage re- 2. De Bari C, Dell’Accio F, Tylzanowski P,
generation and/or to prevent osteoar- Luyten FP: Multipotent mesenchymal 13. Ju YJ, Muneta T, Yoshimura H, Koga H,
stem cells from adult human synovial Sekiya I: Synovial mesenchymal stem
thritis should answer this question. membrane. Arthritis Rheum 2001;44(8): cells accelerate early remodeling of
1928-1942. tendon-bone healing. Cell Tissue Res
2008;332(3):469-478.
Application of Synovial- 3. Jones BA, Pei M: Synovium-derived stem
MSCs for Bone, Tendon, cells: A tissue-specific stem cell for 14. De Bari C, Dell’Accio F, Vandenabeele F,
cartilage engineering and regeneration. Vermeesch JR, Raymackers JM, Luyten
and Muscle Regeneration Tissue Eng Part B Rev 2012;18(4):301- FP: Skeletal muscle repair by adult
311. human mesenchymal stem cells from
Synovial-MSCs may offer an alterna- synovial membrane. J Cell Biol 2003;
tive cell-based treatment strategy for 4. Sakaguchi Y, Sekiya I, Yagishita K, Mun- 160(6):909-918.

April 2013, Vol 21, No 4 259

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