19

Click here to load reader

Approach to cartilage injury in the anterior cruciate ligament-deficient knee

Embed Size (px)

Citation preview

Page 1: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

Approach to cartilage injury in the anterior cruciate

ligament-deficient knee

Andrew S. Levy, MD, Steven W. Meier, MD*

The Center for Advanced Sports Medicine, Knee & Shoulder, Overlook Hospital, 33 Overlook Road/MAC #409,

Summit, NJ 07902, USA

Injuries to the anterior cruciate ligament (ACL)

commonly occur during deceleration pivoting move-

ments. These motions also produce high shear forces

across the cartilaginous surfaces of the knee. When

the ACL tears, there is even further shear stress across

the knee joint and often blunt trauma to the osteo-

chondral surfaces. Consequently, damage to the artic-

ular cartilage has been reported to occur with a

frequency of 15–40% in acute ACL tears [1,2]. In

chronic ACL-deficient knees, the frequency of carti-

lage lesions has been reported to be 79% overall, with

yearly increases from 40% at 1 year to 60% at 5 years

and > 80% at 10 years [3]. The treatment of damaged

articular cartilage remains one of the greatest chal-

lenges facing the orthopedic surgeon today.

Though, classically, ACL reconstruction has been

performed to restore function and prevent instability,

one may now view it as part of the fulmative attempt

to preserve the meniscus and protect the articular

cartilage. It has yet to be shown that ACL recon-

struction can slow the progression of existing chon-

dral lesions or prevent the incidence of new ones, but

a comprehensive approach to repairing cartilagenous

structures at the time of ACL reconstruction hope-

fully will prolong optimal knee function [4,5]. In

order to delineate treatment options regarding artic-

ular cartilage injuries, it is necessary to understand

the biomechanics and biology of healthy and injured

articular cartilage.

Articular cartilage: function

Successful human athletic performance requires

the optimal function of our articulations. Proper joint

function requires not only adequate strength and

stability, but a smooth, gliding articular surface to

allow an effortless range of motion. Dysfunction of

this natural bearing surface results in pain, swelling,

and limitation of function [6]. It has also been known

that injury to this structure may result in progressive

degeneration into osteoarthritis [7].

Articular cartilage: structure

The junction of calcified and noncalcified tissues

has increasingly become implicated as the site of the

essential lesion in articular cartilage injury. The

limited ability of articular cartilage to repair itself

has come under increased scientific scrutiny. Carti-

lage science has blossomed over the past 10 years,

resulting in a dramatic advancement of our under-

standing of the mechanics and anatomy of cartilage

injury. We now have a better understanding of

articular cartilage as a composite tissue with specific

mechanical and physiologic properties.

Articular cartilage consists of a highly specialized

extracellular matrix surrounding a sparse population

of chondrocytes. Chondrocytes are derived from

mesenchymal cells, and it has been demonstrated that

perivascular mesenchymal cells in cell culture can be

recruited to form chondrocytes or osteocytes under

the influence of certain morphogenetic factors [8].

The chondrocytes are responsible for the production

and maintenance of the extracellular matrix. Cartilage

0030-5898/03/$ – see front matter D 2003, Elsevier Science (USA). All rights reserved.

PII: S0030 -5898 (02 )00065 -2

* Corresponding author.

E-mail address: [email protected] (S.W. Meier).

Orthop Clin N Am 34 (2003) 149–167

Page 2: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

is aneural and avascular, leaving chondrocyte viabili-

ty dependent on diffusion of metabolites from the syn-

ovial fluid.

The extracellular matrix in articular cartilage is

responsible for its smooth gliding properties. The

extracellular matrix consists primarily of type 2

collagen, proteoglycans, and water. Type 2 collagen,

which makes up 90–95% of the collagen present in

articular cartilage, is largely responsible for the ability

of cartilage to resist shear stress [9,10].

The proteoglycans present in cartilage consist of

glycosoaminoglycans, including chondroitin sulfate

and keratin sulfate side chains bound to a protein core

to form the aggrecan macromolecule. The protein

core is bound noncovalently to hyaluronate via link

protein to form large aggregates of aggrecan-hyaluro-

nate complexes. Glycosaminoglycans in cartilage con-

tain both carboxy-terminal and sulfated ends, which

are ionized in solution. These ionized groups result

in aggrecan molecules being highly hydrophilic and

account for the swelling pressure of cartilage. As a

pressurized proteoglycan gel with collagen fiber

reenforcement, cartilage is highly resistant to com-

pressive loads.

Articular cartilage is organized into four distinct

layers: superficial, middle, deep, and the calcified

cartilage [11,12]. In the superficial layer, cells and

collagen are arranged in a plane parallel to the joint

surface and proteoglycans are at their lowest concen-

tration. This surface is especially well suited to

facilitate the gliding motion of joints and the large

shear forces acting at the articular surface. The

middle layer has more rounded cells and an oblique

orientation to the collagen fibers. In the deepest layer,

the cell population is at its largest concentration, as is

the proteoglycan concentration. The collagen fibers

in the deepest layer are oriented perpendicular to the

joint surface. Deepest and adjacent to bone is the

calcified cartilage. The calcified cartilage is separated

from the noncalcified deep cartilage layer by an

eosinophilic staining wavy line referred to as the

tidemark. This junction of calcified from noncalcified

tissue has been shown in recent cadaver, animal, and

mathematical models to be a likely source for the

initial injury in cartilage injuries caused by shear

stress [13].

Water molecules are delivered on the surface of

the articular cartilage when a load is applied. The

water is ‘‘squeezed’’ through pores present in the ar-

ticular cartilage. These water molecules add to the

already present synovial-fluid surface film. The fluid-

phase portion of cartilage thus adds to the low friction

surface layer between the two articular surfaces.

Cartilage demonstrates time-dependent deformation

under a constant load: the viscoelastic property of

creep. It is most likely the result of the water

molecules being slowly squeezed out of the proteo-

glycan gel. Water molecules experience drag, how-

ever, as they are squeezed through the porous

collagen fiber network toward the articular surface,

thereby resulting in cartilage’s excellent ability to re-

sist compression. Under normal conditions, cartilage

functions smoothly for decades.

Mechanism of injury

The majority of ACL tears occur through non-

impact rotational deceleration mechanisms.. At the

time of ACL failure, it has been shown that the tibia

can sublux anteriorly and impact the lateral femoral

condyle. Thus, initial ACL disruption also results in

high shear forces across the tibiofemoral articulation.

Additionally, the subsequent instability following

ACL disruption can allow for increased loads to be

transmitted to articular surfaces.

Analytic studies by Mow et al have demonstrated

that articular cartilage behaves as a biphasic material.

Consequently, shear and blunt forces are manifested

at the junction of the uncalcified and calcified carti-

lage [13]. Utilizing this mathematical model, the

authors were unable to derive a situation whereby

shearing forces would produce surface failure (abra-

sion) without first causing damage at the tidemark.

This has been demonstrated in a cadaver model in

which loads with variable speed and force were

applied to femoral condyles [14,15]. The low-speed,

low-energy injuries resulted in injuries below the

articular surface; at the junction of the calcified and

noncalcified tissues. A zone of shear forces radiates

from the impact site, producing injury to the junction

of calcified and noncalcified tissues.

Animal studies have supported this concept.

Where low-energy blows produce selective injury to

the deep structures [14–16], they leave the articular

surface intact. This data implies that the junction

between calcified and noncalcified tissues may rep-

resent the ‘‘weak link’’ in articular cartilage’s ability

to resist shear forces. Transarticular loading of canine

metacarpal-phalangeal joints has resulted in cracks

appearing in the calcified cartilage [17] that went on

to osteoarthritis, thereby strengthening the argument

that injury to the deeper layers may ultimately lead to

articular degeneration. Recently, this phenomenon

has been demonstrated in athletes [18] and in patients

with a history of mechanical symptoms [6,19,20].

Many of these patients demonstrate arthroscopic

evidence of lesions that appeared to have a signifi-

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167150

Page 3: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

cantly larger deep component than the immediately

evident surface lesion. On probing, the uncalcified

tissue appeared to have ‘‘peeled’’ off from the cal-

cified layers.

The correlation between an acute shear-force

injury, such as during disruption of the ACL cartilage

lesions, is not definite. There is increasing evidence,

however, of the poor prognosis of predominant shear-

force injuries [16,18]. Indeed, a reconstructed liga-

ment may restore stability to the knee, but the

prognosis of the articular surface may depend on

factors other than stability [1]. Though an unstable

knee is functionally limiting, it can also lead to

subsequent meniscal injury. Meniscal pathology

resulting in meniscectomy is known to correlate with

joint degeneration, but initially stable or stable recon-

structed knees with intact menisci have also pro-

gressed to joint degeneration [1]. The origin of this

pathology may be the initial, silent insult to the

articular cartilage at the time of ACL disruption.

Additionally, athletes involved in pivoting sports

have developed cartilage lesions without ligament

or meniscal pathology [18]. The high shear forces

at the level of the tidemark in aggressive pivoting

athletes may be sufficient in some situations to induce

injury to the cartilage.

Progression of occult articular cartilage injuries is

an area of active scientific investigation in which

much is yet to be learned. One possible explanation

focuses on the potential space created between the

calcified and noncalcified cartilage at the time of

injury. As the joint is loaded, water molecules may

be delivered to this potential space as the cartilage

undergoes viscoelastic creep [13]. Thus pressurized,

the potential space may expand at the level of the

tidemark with each loading of the joint. Eventually,

the enlarged potential space may communicate with

the joint surface, and a surface lesion will become

evident. When probed, this small lesion will appear to

have delaminated from the calcified tissue, revealing

a much more extensive deep lesion.

Another theory postulates that the biologic

response to injury may result in a construct more

poorly suited to tolerate physiologic loads. A well-

designed animal study found that impulse loading of

rabbit knees resulted in subchondral plate fractures

that healed into a mechanically stiffer construct (via

tidemark advancement) than the normal joint [21].

These joints went on to joint degeneration with time.

Though abrasive and third-body wear does not

appear to cause chondral lesions, it will certainly

result in progression of articular injury and degen-

eration, and, eventually osteoarthritis. Acute injury,

progression of injury, multiple small insults, absent

menisci, alignment, and anatomy are among the

multitude of variables that may eventually result in

osteoarthritis. An articular lesion that progresses or

does not heal could, however, certainly result in a

roughened articular surface that could abrade the

surface with which it articulates.

Thus, disruption of the ACL can either be asso-

ciated with acute chondral injury or can result in

repetitive abnormal joint forces that subsequently

produce additional chondral injury. There may be

damage at the tidemark, furthermore, that may not

be evident at initial clinical evaluation. This may lead

to cartilage deterioration despite stabilization. It is

important, however, to realize that isolated chondral

lesions are often reported in patients who engage in

deceleration maneuvers, and some chondral lesions

found at ACL reconstruction may have been pre-

existing and asymptomatic.

Healing

Injury to the cartilage at either the surface or the

deep layers would not be significant if cartilage had a

strong ability to heal. Unfortunately, cartilage has a

limited ability for self-repair [19,22–31]. Numerous

studies have demonstrated that acutely injured chon-

drocytes respond with the production of collagen and

proteoglycans. This increased matrix production,

however, is insufficient to fill the injured region and

does not result in hyaline cartilage. Furthermore,

chondrocytes lack the ability to migrate into the

adjacent lesion and produce minimal mitotic activity

after adolescence [32].

The primary factor related to cartilage’s poor

healing response is the lack of blood supply to the

chondrocytes. This precludes the formation of fibrin

clot and inhibits the inflammatory cascade that most

tissues utilize in healing [32].

Bone bruises

The association of bone bruises with acute ACL

injury is well recognized. Bone bruises have been

demonstrated by magnetic resonance (MR) imaging in

more than 80% of knees after acute ACL rupture

[33–36]. These injuries typically occur in the lateral

compartment of the knee on the lateral femoral

condyle and posterolateral aspect of the tibia. These

impaction injuries necessarily also involve injury to

the overlying cartilage. Biopsy of the adjacent carti-

lage has demonstrated chondrocyte degeneration and

loss of proteoglycans [37]. The significance of bone

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 151

Page 4: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

bruises and their relationship to chondral defects is not

well understood. An association seems to exist

between severe bone bruises and chondral injury.

Vellet et al described two types of bone bruises, based

on degree of bony involvement, as seen on MR

imaging. Reticular lesions, which occurred in 70%

of patients, are less severe and appear as hemorrhage

and edema in the medullary bone but do not involve

damage to subchondral bone. Geographic lesions,

occurring in 25% of patients, are more severe and

involve signal change contiguous with subchondral

bone. The authors found that the reticular lesions

tended to resolve after 6–12 months, whereas 62%

of the geographic lesions led to ‘‘osteochondral seque-

lae’’ [17]. Spindler et al found that when MR imaging

demonstrated impaction injury to the subchondral

bone with signal change in the overlying cartilage

layer, there was an increased incidence of arthroscopi-

cally apparent cartilage injury with bone bruises on

the lateral femoral condyle [35]. Careful evaluation

with arthroscopic probing of this region is thus war-

ranted at the time of arthroscopy. An association

between bone bruises induced in rabbits and late

degenerative change has been demonstrated. Al-

though this has not yet been shown in humans, it

should be taken into account in return-to-activity

decisions following ACL reconstruction.

Diagnosis

The presence of a chondral lesion may or may not

be known prior to performing an ACL reconstruction.

Physical examination in an unstable knee is not

reliable in detecting chondral lesions. MR imaging

has been shown to have a sensitivity as low as 21%

for detecting chondral lesions [18]. Joint effusion [38]

and the use of intra-articular gadolinium [39] have

been shown to increase the rate of detection, but MR

imaging, nevertheless, remains an unreliable diag-

nostic tool in identifying these lesions. Though

new MR imaging techniques (3D-SPGR) have

reported increased resolution of cartilage, sensitivity

for detecting chondral lesions remains poor (62%,

dependent on lesion location and grade), and their

availability to most clinicians limited. In the future,

imaging techniques that actually detect biochemical

and biomechanical changes and matrix degeneration

may increase sensitivity [40,41]. Because the current

gold standard for identifying chondral lesions is the

arthroscopic viewing and careful probing of articular

surfaces, many of these lesions that coexist with ACL

injury are often first diagnosed at the time of the

definitive ligament reconstructive procedure. This

fact can be used to illustrate the importance of the

surgeon’s need to be prepared to address a possible

chondral lesion each and every time an ACL recon-

struction is performed.

Following successful ACL reconstruction, occult

chondral injuries that were not apparent at the time of

reconstruction may produce persistent symptomatol-

ogy. Patients with articular cartilage lesions may

present with a myriad of confusing signs and symp-

toms, but the most common complaint is knee pain.

The pain is generally intermittent and may or may not

have been related to an additional injury. The pain

may be reproducible with certain activities or within a

specific arc of motion [18]. Mechanical symptoms of

popping, locking, and catching may occur if a frag-

ment has broken loose or a flap of delaminated

cartilage is present. Physical examination should

proceed with thorough inspection of the knee and

alignment, palpation of structures, range of motion

testing, and evaluation of joint stability. Special

attention should be paid to the joint line and femoral

condyles because tenderness may be present if a

lesion extends far enough anteriorly to permit palpa-

tion. Clinically evident joint effusion is present in

only about 30% of patients, though swelling is a

common complaint. Joint crepitation may be present

but in only 25% of patients [18]. Lesions in the

patella-femoral joint are more difficult to identify.

The patella-femoral grind and quadriceps resistance

tests are sometimes helpful. These lesions can easily

be mistaken, however, for anterior knee pain syn-

drome, patellar instability, chronic chondromalacia,

or early patella-femoral osteoarthritis [6]. Although

history and physical examination can reveal some

cartilage lesions, they are sometimes difficult to

identify. The key to making the diagnosis is to

maintain a high index of suspicion.

Numerous classifications have been published

describing the appearance of chondral lesions [6,20,

42–46]. It is critical, however, to note that most of

these classifications involve not only visualizing the

articular surface but also noting the consistency of the

cartilage when arthroscopically probed. Essentially,

most classification schemes describe lesions, either

open or closed. Closed lesions are simply the softening

of the cartilage on probing, with or without surface

changes. Open lesions are classified according to size

and depth of involvement. Full-thickness lesions

involve true exposed subchondral bone, whereas par-

tial-thickness lesions may involve only the layers

superficial to the calcified cartilage. Larger and deeper

lesions obviously have a worse prognosis.

Arthroscopy is invaluable in the evaluation of

articular cartilage lesions in that it allows direct

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167152

Page 5: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

visualization and classification of the lesion. Coin-

cident meniscal or ligament pathology can be ad-

dressed, and, if amenable, the chondral lesion can be

treated at the same operative sitting. If a more

extensive lesion is found, accurate assessment of the

pathology can be attained, thus permitting the patient

and physician to pursue an objective evaluation of the

various more-complicated treatment options.

Treatment

Nonoperative treatment

Nonoperative treatment of chondral lesions asso-

ciated with ACL injuries is relevant only in the knee

with post-ACL reconstruction status. In most cases, a

course of nonoperative treatment should be instituted

for at least 12 weeks in suspected chondral lesions

before surgical intervention is contemplated. Closed

chain-muscle strengthening combined with cryother-

apy and oral anti-inflamatories are the mainstay of

this treatment. Supportive braces (ie, elastic or neo-

prene) often assist in controlling effusions and are felt

to be beneficial by many individuals with chondral

lesions. Open chain strengthening may be used in

some cases when the work can be performed outside

the painful arc of motion. Intra-articular cortisone

injections are contraindicated in athletes because of

the direct deleterious effect on the articular chondro-

cytes and the potential for additional knee injury.

Hylauronate injections may be helpful, though no

data exist on their use in focal chondral lesions. No

data exist concerning the success of nonoperative

treatments in patients with chondral lesions.

Surgical treatment

The ultimate goal in the surgical treatment of

articular cartilage lesions is the reproduction of viable

hyaline cartilage bound to a restored subchondral bone

plate and the surrounding hyaline cartilage. The

achievement of this goal implies that arthritic deteri-

oration is prevented and reversed with resumption of

full asymptomatic function. At present, these goals

remain elusive and successful treatment has been

directed toward reduction of pain and swelling and

improved function. Additional difficulties exist in

comparing animal studies of articular cartilage. The

animal models used often have articular cartilage

properties that are extremely different from those in

human cartilage, and the lesions created rarely

resemble the human condition. The outcomes of these

studies have been based, furthermore, on the surgeon’s

ability to fill the cartilage defect with hyaline-like

cartilage. No evidence exists to suggest that tissue that

is more hyaline-like will diminish pain, improve

function, and prevent deterioration of the joint.

The operative treatment of chondral injuries of the

articular surface can be divided into four basic

principles. In advanced articular cartilage destruction,

(ie, varus collapse in ACL-deficient knee), the alter-

ing of joint forces may be utilized to decrease pain

and improve function. In isolated chondral lesions,

treatment includes stabilization of loose or worn

articular cartilage, plus either stimulation of a repair

process derived from the subchondral bone or regen-

eration of an articular surface (via transplantation of a

cell line or precursor tissue into the defect). In many

cases, a treatment option will include a combination

of different techniques.

The anatomic location of the lesion must be taken

into account when treating chondral lesions. This is

most true of the patellofemoral joint where most

lesions are the result of lateral patellofemoral com-

pressive forces such as tilt and subluxation. In these

cases, all surgical cartilage treatment options are

likely to fail if the underlying mechanical problem

is not addressed. Different areas within the joint,

furthermore, are not easily accessible for many treat-

ment options. Once the surgeon is aware that a

chondral lesion exists, he or she must select the most

appropriate technique for treating it.

Cartilage stabilization and debridement

The pain associated with chondral lesions is

attributed to the free nerve endings found in the

subchondral bone and the effects of cartilage debris-

mitigated effusions [13,46]. Consequently, the

removal of debris from the joint is performed to

diminish its irritative effects on the synovium. This

may be achieved either through lavage or direct

particulate removal. The exact mechanisms whereby

isolated chondral lesions irritate free nerve endings in

subchondral bone are unknown. This may be attrib-

uted, however, to unstable chondral flaps producing

mechanical irritation of the subchondral plate. Stabi-

lization of the walls of the chondral lesion is thus

performed. Unfortunately, the term ‘‘stable’’ has not

been well defined, and one must be careful to avoid

completely ‘‘peeling the orange’’ and removing

excessive amounts of cartilage. Several authors

[18,20] have demonstrated that the visible chondral

lesion averages approximately one third of the site of

the final lesion once debridement is concluded. Addi-

tional data exist to suggest that tapering chondral

edges is less mechanically advantageous than main-

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 153

Page 6: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

taining vertical chondral lesion walls [43]. In the

isolated chondral lesion, stabilization and debride-

ment are the initial preparatory phase in treatment.

Traditionally, debridement has been performed me-

chanically with the use of rotary power shavers or

other hand instruments. Mechanical debridement with

rotary shavers is relatively easy and does not require

unusual or expensive equipment. It may lead to exces-

sive removal of normal cartilage, however, or leave

an unstable margin that can continue to propagate.

We have found that liberal debridement with bent

curettes and osteotomes can eliminate unstable edges

effectively in focal defects without jeopardizing the

surrounding surface.

Thermal modification—coblation chondroplasty

In theory, thermal modification is an attractive

alternative to mechanical debridement because it

allows for more precise ablation of smaller amounts

of tissue. ‘‘Tissue welds’’ can be accomplished,

eliminating residual unstable free edges that may be

prone to propagation.

Lasers (light amplification by stimulated emission

of radiation) are used in orthopedics to produce an

intense beam for cutting, coagulating, and ablating of

tissue. This occurs because of the absorption of laser

energy and its subsequent conversion to heat based

on the water content of a given tissue. In the late

1980s, surgeons began applying the thermodestruc-

tive effects of the laser to damaged articular cartilage.

The use with articular cartilage lesions achieved

prominence in 1989 when some investigators claimed

that the holmium laser could be used to stimulate

hyaline cartilage formation. [46].

Further research has questioned these findings and

also suggested that the penetration of laser energy is

deeper than once thought, and that there is a delayed

zone of cartilage destruction that occurs after the

initial laser use. This area is more extensive than

the initial zone of visible damage [47]. Immediately

after 0.5 J/Pulse laser treatment of full- (5 pulses) and

partial-thickness (1–2 pulses) defects in sheep, a

zone of damage was noted extending up to 500

microns below the ablation crater. At 2- to 4-weeks

postlaser surgery, hyperchromatic nuclei were seen

up to 800 to 900 microns distal to the ablation crater,

and loss of osteocytes was noted in the subchondral

bone. There was no healing of partial-thickness

lesions, but some fibrocartilaginous healing was

noted in the full-thickness defects. Ten weeks post-

laser treatment, no repair tissue was left in the full-

thickness lesions and no repair response had occurred

in the partial thickness lesions. Granulation tissue was

present in the damaged subchondral bone, but not in

the chondral ablation crater. This increased damage

with time is attributed to a photo-acoustic effect.

Further concerns regarding the use of lasers on

articular cartilage arise because of the growing num-

bers of reports of laser-induced avascular necrosis of

the femoral condyles. At present, there is little evi-

dence to suggest that laser use will produce hyaline

repair, and its use is not advised in the treatment of

focal chondral defects.

Radiofrequency

The use of radiofrequency (RF) has proliferated

recently in orthopedics for various applications in

tissue modification such as capsular and ligamentous

shrinkage and debridement of meniscal and chondral

lesions. RF works by generating ultrasonic waves that

produce heat as they pass through the target tissue.

This heat results in the denaturing and shrinkage of

collagen fibers. Both monopolar RF (MPRF) and

bipolar RF (BPRF) devices are commercially avail-

able. RF has been used to debride meniscus tears and

chondral defects by ablating the tissue flaps and

rough edges associated with these lesions. An attract-

ive feature is the ease of accessing hard-to-reach areas

with the compact RF probe where mechanical

debridement may be difficult. Another feature that

makes RF popular is its ability to virtually ‘‘melt’’ or

‘‘weld’’ fragmented tissue to a stable margin. This is

theoretically attractive when dealing with certain

chondral lesions to avoid the excessive ‘‘peeling the

orange,’’ as mentioned, that can be associated with

mechanical debridement (Fig. 1).

The concern about this technique is that it could

cause residual thermal damage to the surrounding

Fig. 1. Thermal coblation of patella chondromalacia with

radiofrequency.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167154

Page 7: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

cartilage and subchondral bone and possibly lead to

progression of cartilage degeneration or perhaps even

osteonecrosis. Lu reported on the effects of MPRF on

partial-thickness cartilage lesions in sheep and found

that, though the appearance of the treated surfaces was

more smooth when compared with mechanical

debridement, scanning electron microscopy revealed

significantly more chondrocyte death in the RF group.

Studies show that RF induces changes resulting in

decreased chondrocyte viability, and progressive loss

of proteoglycan over time [48,49]. Theoretically,

BPRF should cause less collateral damage than MPRF

because the current flows from electrode to electrode

at the probe tip in contrast with monopolar current

which travels from probe tip, through the patient, and

to the grounding pad. Current studies do not substan-

tiate this, though. Kaplan performed a study, support-

ing the use of BPRF, with fresh human cartilage from

total-knee arthroplasty specimens using hematoxylin

and eosin staining and found that the chondrocytes

remained in their lacuna when analyzed 6 hours post-

trauma [50]. Lu et al, however, did a similar study

with confocal laser microscopy and vital cell staining

because they felt that light microscopy did not evalu-

ate chondrocyte viability effectively. This study

revealed chondrocyte death to a depth of 1.5 mm to

2.5 mm. Depending on the degree of articular thinning

in the particular specimen, this sometimes involved

penetration all the way down to subchondral bone

[51]. Recent forthcoming work by Markel also shows

BPRF creating significant chondrocyte death, even to

a greater extent than MPRF.

Depth of penetration has been shown to be depen-

dent on temperature, duration, and tissue quality.

The collagen denaturation and shrinkage desired

for annealing chondral surfaces begins to occur at

65�Celsius, whereas chondrocyte death occurs at only45�. Exposure times of 5 seconds with MPRF have

been shown to create cellular destruction comparable

to mechanical debridement, but at least 15 seconds of

treatment may be required to smooth the surface

adequately, doubling the depth of cellular death [52].

Moller et al has shown that the more extensive the

chondromalacia, the greater the vulnerability of the

cartilage to thermodestructive effects [53]. This sug-

gests that the undesirable effects of RF may be more

pronounced in the very lesions it is used for most. Stein

et al have shown that, after 1 year, electocautery

chondroplasty actually produces inferior clinical

results in grade 3 and 4 chondromalacia when com-

pared with mechanical debridement [54].

We feel that radiofrequency coblation has a limited

role in cartilage debridement. It may be appropriate

for patellar chondromalacia where partial-thickness

fibrillation can be extensive and full-thickness chon-

drocyte death may be avoided because patellar carti-

lage is particularly thick. Great caution should be

exercised, though, when considering the use of these

devices on condylar lesions where cartilage typically

is thinner.

Marrow-stimulating techniques

Several different marrow-stimulating techniques

(MST) have been described, and they involve the

stimulation of a fibrocartilage repair response by

accessing vascular channels through mechanical pen-

etration of the subchondral bone [33–60]. The lesion

first fills with blood, creating a hematoma and result-

ing in the production of a fibrin clot [24,25]. This

allows migration of mesenchymal precursor cells.

Early on, hyaline-like cartilage with a high proportion

of type 2 collagen may be found in the repair matrix

[61]. Over time, however, type 1 collagen becomes

more prevalent, resulting in a fibrocartilage fill of the

lesion [26]. No evidence exists to suggest that the

fibrocartilage binds to the surrounding normal hya-

line cartilage. It is theorized that the fibrocartilage’s

beneficial effect is caused by its ability to seal over

the lesion, thus diminishing mechanical stress on the

subchondral bone. This same sealant effect may also

reduce joint effusions by diminishing cartilage debris

from floating free into the joint [24].

Techniques of cartilage repair include abrasion,

drilling, and ‘‘microfracture’’. These techniques vary

mainly in their method of achieving subchondral

penetration. All of these techniques first employ

chondral stabilization and debridement as part of

the procedure. A significant advantage of these tech-

niques is that they can all be performed arthroscop-

ically on an outpatient basis with minimal morbidity

to the patient.

Cartilage lesion abrasion is differentiated from

abrasion arthroplasty in that, in chondral lesion

abrasion, only the base of an isolated chondral lesion

is abraded to penetrate the subchondral bone and

stimulate punctate bleeding. Abrasion arthroplasty

has been described in arthritic patients as a diffuse

deep abrasion of entire joint surfaces to produce a

massive bleeding bone surface. By contrast, abrasion

of a chondral lesion usually employs a shaver rather

than a burr to minimize deep penetration of the

subchondral bone. Short-term data (1–2 years) has

demonstrated that this technique is effective in

athletes in diminishing symptomatology and permit-

ting a return to competitive sports at approximately

10 to 12 weeks [18]. Most athletes did note persist-

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 155

Page 8: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

ence of dull aching pain after strenuous activity. The

overall relief of symptoms in this athletic population

was comparable to the preliminary data published

on the results of cartilage cell transplant in non-

athletes [62].

Another common way of penetrating the subchon-

dral bone at the base of a chondral lesion is through

drilling. Theoretically, this technique preserves part

of the calcified cartilage layer while creating vascular

channels to allow bleeding from the subchondral

bone. There are two basic concerns with this tech-

nique. The first is that the speed of the drill may

generate excessive heat and produce localized osteo-

necrosis. The second is that the vascular channels

themselves result in columns of fibrocartilage that

adversely effect later treatment options [63]. In a

single report of this technique via open arthrotomy,

patients returned to full activity at 6 months with 69%

rated as good, 3% fair, and 28% poor [43].

Another alternative technique for cartilage repair

involves the use of specially designed ‘‘awls’’ to make

perforations in the subchondral bone (Fig. 2). Light

arthroscopic shaving to remove debris follows. The

theoretical advantage of this microfracture technique is

that access to undifferentiated mesenchymal cells is

provided without the drawbacks of drilling. Though no

clinical studies of this technique have been published,

the inventors have presented early animal data on the

technique. In horses, microfracture technique gener-

ated 50% more type 2 collagen than controls and

demonstrated 60% to 90% fill of full-thickness lesions.

The inventors have also compared this technique with

deep abrasion in horses. Six weeks after treatment, the

microfracture group lesions were noted to have a more

hybrid cartilage fill that was felt to be more hyaline-

like than that of the deep abrasion group [64].

Favorable short-term results of MST have been

reported. Steadman has reported reduction in pain,

Fig. 2. (A) Chondral lesion. (B) Chondral lesion after debridement and establishment of a stable border. (C) Chondral lesion after

microfracture. (D) Fibrocartilage ingrowth one year later.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167156

Page 9: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

swelling, and improved function with an average

follow-up of 6 years [65]. Longer-term results may

not be as satisfactory, however. Fibrocartilage lacks

proteoglycan concentration and is thought to be less

durable than themore desireable hyaline cartilage [61].

There are no long-term comparative studies on MST

but clinical results probably deteriorate over time

because of the poor wear characteristics of fibrocarti-

lage. Limited studies on abrasion arthroplasty dem-

onstrate some temporary symptomatic relief but these

beneficial effects do not last beyond 2 to 4 years

[66,67]. Examination of failed repairs has revealed

soft, fibrillated tissue with central degeneration [68].

MST remains the standard by which other tech-

niques are measured. Advantages of this method

include its ease of use, low cost, low morbidity,

ability to be performed arthroscopically as an out-

patient procedure, and no contraindications with the

technique based on lesion size or location. Smaller

and relatively acute lesions in the femoral condyle

and trochlear areas tend to respond best [69]. Dis-

advantages to this technique are the prolonged post-

operative period of restricted weight bearing and low

durability of repair tissue. Biomechanically, fibrocar-

tilage is markedly inferior to normal hyaline cartilage

in response to shear and compressive stress [70].

Combined with the stress riser between the fibro

and hyaline cartilage, this makes survivability ques-

tionable over long periods of time. The predictability

of a successful outcome of fibrocartilage producing

treatments may be quite variable in different patients.

Autogenous osteochondral grafting

The rationale behind autogenous osteochondral

grafting (AOG) is the vast array of analytical, cada-

ver, animal, and (recently) human data demonstrating

that the common essential lesion in the development

of chondral lesions occurs at or near the tidemark

where the subchondral plate (subchondral bone and

calcified cartilage) interfaces with the uncalcified

cartilage. By replacing the entire osteochondral unit,

one could theoretically address and remove the actual

site of damage that has led to the visible lesion.

The first known report of transplanting articular

cartilage bone fragments was by Judet in 1908 for the

treatment of osteochondritis descicans [71]. In 1959,

Campbell et al reported using fresh osteochondral

autografts with little or no destruction occurring over

the first year [72]. In 1961, Pap and Krompecher

reported the transplantation of articular cartilage frag-

ments and their associated < 5 mm of subchondral

bone in 51 dogs. They noted survival of the articular

cartilage of up to 2 years provided normal physio-

logic loads were applied [73]. In 1962, Entin per-

formed autogenous osteochondral transplantation

from the foot to the hand and found that the cartilage

was not replaced [74].

In 1963, Campbell again reported on the use of

osteochondral grafting on 42 dog knees. In this study,

grafts were limited to 1 cm wide � 2 cm long, with

subchondral bone depth limited to < 5 mm [75]. They

noted that the osseous portion healed by 14 days via

creeping substitution, and that the articular cartilage

appeared grossly and histiologically normal at 2 years

postgrafting. They did note, however, that the articular

cartilage of the grafts did not bind to the surrounding

cartilage. They also speculated that increasing the

depth of the subchondral bone might lead to increased

necrosis of deep bone.

The healing of osteochondral autografts has been

further studied by McDermott et al [12]. It appears

that the surface osteocytes in the subchondral bone

survive, whereas those deeper than 3 mm are replaced

within the first 4 weeks.

Limited biomechanical studies have also been

performed to evaluate the effects of graft size on

function. It has been shown that a 15% increase in

diameter results in a 50% increase in torsional

strength of the grafts [76]. The potential unknown

effects of radius mismatch must temper this, however.

In 1994, Hangody reported on a technique termed

‘‘mosaicplasty’’ [77]. Mosaicplasty utilizes multiple

plugs of autogenous osteochondral graft to fill chon-

dral lesions. This procedure was performed on

122 humans. There were 57 medial femoral condyle

lesions, 48 lateral femoral condyle lesions, and

17 patella lesions with > 1 year follow-up. The

lesions ranged from 1 to 8 cm2 and grafts varying

from 2.7 to 4.5 mm diameter were obtained from the

lateral and medial edge of the condyles to fill the

defect via an open arthrotomy. At 1 year follow-up,

there were no cases of loosening or backing out of

the grafts and the average Hospital for Special

Surgery (HSS) score was 88.4 (range: 61–100).

Second-look arthroscopy was performed in many

cases and showed good congruency.

A prospective multicenter study was initiated to

follow up 200 patients for 5 years. Lesions treated

averaged 143 mm2 (range, 80–25 mm2). A total of

81% were performed arthroscopically, with 19%

requiring miniopen technique. So far, patients reported

improvement with the technique, and no deterioration

of results has been noted at 2-year follow-up [78].

The use of osteochondral autografts has also been

described in conjunction with ACL reconstruction. In

29 cases, 1- to 1.5-cm defects of the femoral condyles

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 157

Page 10: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

were filled with osteochondral plugs (5 mm wide �10–15 mm long) harvested from the intercondylar

notch. At 2 to 3 years post-transplantation, the articular

cartilage on the transplants appears (via MR imaging

and probing) to have survived. The surrounding area is

filled with fibrocartilage. Clinically, this has correlated

with 19 excellent outcomes in 22 cases [79].

The resurgence in enthusiasm for osteochondral

grafting is associated with the increased development

of techniques that permit more predictable arthro-

scopic harvesting and delivery of the plugs. This,

however, applies only to limited areas of the femoral

condyles. The use of this technique on the patella,

trochlea, and posterior femoral condyles requires open

arthrotomy. Additionally, the treatment of defects

greater than 12 mm in diameter also require open

arthrotomy to ensure perpendicular graft placement.

Advantages of this technique include preservation

of hyaline cartilage, relative low cost, and the ability

to be performed arthroscopically as an outpatient

procedure in a single stage. Postoperative limitations

are less restrictive than the other techniques, requiring

only a few weeks of protected weight bearing. The

results appear to be at least comparable with MST in

the short term.

There are several disadvantages to this technique.

First of all, it is technically demanding and requires

advanced skill to be performed correctly. Obtaining

perpendicular graft harvesting and placement is crit-

ical, along with reproducing an accurate radius of

curvature. Very large lesions exceed the amount of

available graft tissue. Generally, defects < 2.5 cm in

area are most appropriate for this technique to not

surpass the capacity of graft sources. There are limi-

tations based on lesion location, and this method is not

recommended for patellar or tibial lesions. Far poste-

rior femoral defects are difficult to access with current

instrumentation. The harvesting of autologous graft

tissue necessitates a certain degree of graft site mor-

bidity, although very little is known about this. There

seems to be negligible graft site morbidity in the short

term, but no long-term studies have been done to re-

veal potential long-term adverse effects. Simonian et al

measured contact pressures throughout the knee and

determined that there are no true nonweight-bearing

areas of the knee, although the supero-lateral aspect of

the lateral femoral condyle above the sulcus terminalis

and the supero-medial area of the intercondylar notch

showed significantly less contact pressure [80]. Other

issues with this technique include cartilage thickness

mismatch, graft impaction forces, fibocartilaginous fill

around the plugs, and potential remaining stress riser

production between the two nonbinding cartilage sur-

faces. Multiple small plugs allow better radius curva-

ture matching versus a single large plug, but each graft

will be weaker in torsional strength, and more suscep-

tible to delamination during impaction. Grafts > 8 mm

in diameter raise concerns with harvest morbidity and

radius mismatch. Our preferred plug size is 6 mm.

Overall, autologous osteochondral grafting pro-

vides a very reliable means of reestablishing viable

hyaline cartilage to a lesion site (Figs. 3, 4).

Allograft osteochondral grafting

The use of osteochondral allografts for tumor

treatment dates back to the 1950s. In 1959, Campbell

et al reported using fresh osteochondral autografts

with little or no destruction occurring over the first

year [72]. When fresh and frozen allografts were

used, however, they became fibrillated and degener-

ated within a few months.

The important issues with osteochondral allograft-

ing include chondrocyte viability, graft incorporation

and remodeling, host immune reaction, and potential

for disease transmission. Historically, osteochondral

allografts were implanted ’’fresh’’ within 1 to 2 days of

harvesting. This presents certain logistical difficulties

as the patient and surgeon have to be ‘‘on call’’ if a

donor should become available. This also does not

allow sufficient time to process and screen specimens

adequately for disease transmission risk. As time

elapses after harvest, chondrocyte survivability dimin-

ishes progressively. It is not known what critical

percentage of viable chondrocytes is necessary for

optimal long-term durability of implanted cartilage,

but it is intuitive that lack of active chondrocytes will

lead to eventual cartilage degradation. Preservation

methods such as fresh freezing, freeze-drying, and

cryopreservation have been studied to prolong the

shelf life of specimens, but all have inferior results

when comparedwith fresh grafts [81,82]. Chondrocyte

survival has been improving, however, with newer

two-stage cryopreservation techniques. Cryoprotec-

tant use has subsequently produced 85% to 95%

chondrocyte survival rates with maintenance of chon-

drocyte phenotype [83].

Typically, osteochondral tissue has been consid-

ered ‘‘immunologically privileged’’ because many

believe that it does not generate a host-immune

response. Certainly, chondrocyte antigens have been

shown to be shielded from the humoral circulation by

cartilage matrix, allowing them to avoid recognition

by the host-immune system [84]. Though overt tissue

rejection does not occur as it would in soft tissue

organ transplantation, such as the heart or liver, which

requires immunosuppressive therapy, more subtle

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167158

Page 11: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

tissue incompatibility processes may still be occur-

ring. There is evidence to suggest that the bone

marrow elements are capable of generating a cell-

mediated host response that may impair graft incorpo-

ration and remodeling [85].

A major factor associated with the poor results of

osteochondral allografts appears to be related to the

normal remodeling of the cancellous bone. The

deterioration of the articular cartilage in allografts

appears to occur as a result of subchondral collapse

produced by bone turnover in the metaphysis [12,86].

Thus, the fate of the transplanted articular cartilage in

allografts is related to the fate of the subchondral

bone. It appears that for an allograft cartilage trans-

plant to be successful, the allograft must heal to the

surrounding bone incompletely so that extensive

Fig. 3. (A) Schematic of graft/inserter placement. (B) Schematic of final impaction of graft. (C) Schematic of final graft

placement. (From Levy AS. Osteochondral autograft for the treatment of focal cartilage lesions. In: Cole BJ, editor. Operative

techniques in orthopaedics, vol. 11, no. 2. Philadelphia: WB Saunders; 2001. p. 110–111.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 159

Page 12: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

revascularization and resorption does not result in

cartilage collapse.

To date, no studies exist that address the use of

modern osteochondral grafting techniques for allo-

graft. Theoretically, if successful, this would improve

graft thickness and radius of curvature mismatch

concerns in autograft techniques.

We feel that,with all the limitations currently

facing osteochondral allografting, it should not be

considered an initial treatment of choice. It is a major

Fig. 4. (A) Osteochondral grafting, chondral lesion. (B) Osteochondral grafting, roaming recipient site. (C) Placing graft in

recipient site. (D) Three osteochondral grafts in place. (E) Second look, 1-year later.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167160

Page 13: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

reconstructive procedure that precludes all other repair

techniques. If the graft fails, the fall-back procedure

becomes prosthetic arthroplasty. In keeping with our

philosophy of not ‘‘burning bridges’’ whenever pos-

sible, we would consider osteochondral grafting a

salvage procedure and not for initial treatment.

Autologous chondrocyte reimplantation

Cartilage regeneration implies the transplantation

of functional cells or precursor cells into the defect.

Regenerative techniques include autogenous peri-

chondral transplant, autogenous periosteal transplant,

and autogenous chondrocyte transplant.

Rib perichondrium has been utilized in an attempt

to fill osteochondral lesions in young patients. Its use

has not been documented in isolated chondral lesions.

Early success in osteochondral lesions did not persist

because of the high propensity for perichondrium to

calcify. Its use is not recommended in chondral lesions.

Periosteum is plentiful throughout the body,

although its thickness diminishes with age. Several

studies have demonstrated that the cambium layer of

periosteum can differentiate into chondrocytes and

form hyaline cartilage [7]. When sutured to the base

of a lesion, a hyaline-like repair tissue was formed

with similar histiologic characteristics (87% type 2

collagen) and biomechanical characteristics as normal

hyaline cartilage. The use of continuous passive

motion (CPM) has been found to be advantageous

in increasing the success rate of periosteal transplanta-

tion in animals [87]. Preliminary data has demonstra-

ted the efficacy of this technique in reducing pain in

lesions of the patella and the femoral condyle [88].

Controversy exists as to whether the periosteum is

best placed with the cambium layer facing into the

joint [87–89] or into the lesion [20,21].

The advantages of periosteal transplant are that the

supply is virtually unlimited and that minimal instru-

mentation and commercial supplies (cell culturing) are

required. Unfortunately, the promising early results of

periosteal transplant to the femur appear to diminish

with time [90]. Patient morbidity is fairly high, as this

requires a formal arthrotomy and prolonged CPM.

Additional concerns exist as to the fact that the

cellularity of the periosteal harvest appears to be

closely related to the experience of the harvester [90].

In order to augment the periosteal transplantation,

in 1989, Grande et al reported placing cultured auto-

genous chondrocytes under periosteum sutured

directly to the surrounding hyaline cartilage. In rabbit

defects, this was found to produce greater filling of the

defects than in controls (periosteum alone sutured to

cartilage). Histologically. this repair tissue was felt to

be significantly more hyaline-like than the controls. In

1995, Brittberg et al reported on the results of this

technique in 23 human subjects [62]. They reported

eight good (occasional pain and swelling), six excel-

lent, and two fair, with poor results on femoral lesions

1 year post-transplant. Patellar lesion treatment did not

perform as well—yielding two good results, three fair,

and two poor. Arthroscopic second looks revealed that

there was soft repair tissue in the defects without

incorporation into the surrounding hyaline cartilage.

This conflicted with the data from previous studies that

showed early degeneration at 12 weeks post-transplant

[91]. These improved results were attributed to

changes in postoperative regimen.

Recently, long-term follow-up has been reported

by Peterson et al with a group of 61 patients who

have been treated with autologous chondrocyte

implantation (ACI) for femoral and patellar lesions

[76]. These researchers found that 82% of patients

had a good/excellent result after 2 years, and 84% had

a good/excellent result after 5 to 11 years. They

concluded that most failures occurred within the first

two years of surgery, and that if patients had good

function at 2 years, they would most likely continue

to do so. This suggests that successful ACI results in

durable regenerated tissue. In 8 of 12 patients, biopsy

of regenerated tissue revealed hyaline-like matrix

composed primarily of type 2 collagen, well anchored

to the subchondral bone. The remaining biopsies

were predominantly fibrous in nature.

Recent data from the Cartilage Repair Registry

reveals that 81.8% of patients who had ACI for

femoral lesions were significantly improved after

6 years [92]. Medial femoral condyle lesions were

most numerous, and 70% of these patients experi-

enced improvement. Lateral femoral condyle and

trochlear lesions tended to do better but presented

relatively infrequently. The function of improved pa-

tients was typically assessed as ‘‘good’’ because there

were no ‘‘excellent’’ ratings. The majority of these

patients, however, were rated as poor prior to im-

plantation, and ACI was often used as a salvage treat-

ment in very severe cases. Most frequently, reported

adverse events include hypertrophic repair tissue and

intra-articular adhesions.

Enthusiasm for this technique in the United States

has been hampered by theoretic and economic con-

cerns. This staged procedure is invasive and requires a

formal arthrotomy. It is also expensive and requires

prolonged postoperative limitations. Expectations in

this patient group tend to be more modest and directed

toward returning patients to activities of daily living as

opposed to sports. This may be because this technique

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 161

Page 14: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

is often employed in patients with severe conditions

involving very extensive disease and history of pre-

vious failed surgery. Recent follow-up provides prom-

ise for this technique, however, in properly selected

patients. Use of this technique in younger ACL-injury

patients with large lesions in knees that are otherwise

relatively intact may produce more good-to-excellent

results and make returning to sports a realistic

expectation (Fig. 5).

Cartilage stimulation via growth factors

An exciting area of cartilage repair and regenera-

tion involves the use of growth factors. These poly-

peptides attach to chondrocyte cell surface receptors

(integrins) and influence matrix production, prolifera-

tion, and migration and replication [7]. The two most

promising factors at present are insulin-like growth

factor I and transforming growth factor beta. These

have been shown to enhance matrix synthesis in

animal studies. Unfortunately, these growth factors

are not specific for chondrocytes and can affect an

entire joint adversely. Further research is needed into

delivery, regulation, and modulation of these factors

before they are utilized in human joints.

Authors’ preferred treatment

Symptomatic lesions require treatment. The pres-

ence of a symptomatic chondral lesion may or may

Fig. 5. (A) Delamination of chondral lesion. (B) Autologous chondrocyte reimplantation. (C,D) One-year follow-up—hyaline

cartilage ingrowth.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167162

Page 15: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

not be known prior to ACL reconstructive surgery.

When physical findings of pain, joint line tender-

ness, and catching or locking are present, it is

seldom clear whether meniscal or chondral patho-

logy or both are responsible. As previously stated,

MR imaging is of limited benefit as chondral lesions

are identified by MR imaging in only a minority of

cases. MR imaging is fairly sensitive in detecting

meniscal tears, but the mere presence of a meniscus

tear on a preoperative scan does not preclude a

coexistent chondral lesion that may be causing either

a portion or all of the symptoms. Certainly, a normal

appearing MR image in the presence of mechanical

symptoms is even less helpful. A symptomatic

lesion can be considered one whose existence is

apparent on arthroscopic viewing in a patient with

the appropriate preoperative signs and symptoms.

Treatment options in this context include MST,

AOG, or ACI.

Alternatively, chondral lesions may be found in

patients with no preoperative mechanical symptoms.

We believe that asymptomatic lesions discovered

incidentally at the time of arthroscopy for ACL

reconstruction should be treated with at least a

marrow-stimulating technique. There is very little

disadvantage to this approach in that it does not

‘‘burn any bridges.’’ Minimal additional morbidity is

incurred, and any of the more extensive chondral

resurfacing techniques can still be performed at a

later date if the need arises with no adverse effect.

ACL injury patients are typically very active and

place high demands on their knees. Even though

researchers have not been able to prove that cartilage

repair or regeneration has any effect on the devel-

opment of degenerative change in the knee, it makes

sense that some attempt should be made to address

the deficient articular surface in this setting, particu-

larly if the additional procedure adds very little in

the way of morbidity. If lesions are on the central

and anterior third of the femoral condyles, the

surgeon may be justified in performing an osteo-

chondral graft. The harvesting of up to three plugs

from the lateral notch can be performed as part of

the notchplasty.

Postoperatively, the ACL protocol needs to be

modified. Early active range of motion, exercise

bicycle, and isometric quadriceps exercises are ini-

tiated while the limb is kept nonweight-bearing for

3 weeks. From 3 to 6 weeks, partial weight bearing

is initiated. After 6 weeks, the patient is advanced to

full weight bearing, and strengthening exercises are

instituted. Sports-specific rehab is initiated at 10 to

12 weeks with full return to activities based on a func-

tional assessment.

MST for a chondral lesion should not be termed a

treatment failure until symptoms continue for at least

6 months postop. If pain and/or swelling persist and

function is diminished, consideration can be given to

a salvage procedure. In salvage situations, it is

important to allow the subchondral plate to recover

from the initial surgery. Once a patient has failed a

less-aggressive treatment option, our preference is to

perform an ACI technique for lesions of the femoral

condyle and trochlea. It is important to begin prepar-

ing the patient for this procedure and its implications

prior to harvesting the chondrocytes for culture. If

this is unachievable for socioeconomic reasons, con-

sideration is given toward osteochondral grafting via

a formal open arthrotomy.

ACL-dependent scenarios

ACL surgery with known chondral lesion

The presence of a chondral lesion after acute ACL

injury may be known to the surgeon if it is visible on

MR imaging. In this scenario, the physician has plenty

of time to plan addressing the chondral lesion at the

time of ACL reconstructive surgery and to counsel the

patient appropriately. The surgeon may choose from

MST, AOG, or ACI depending on the size and

location of lesion. If AOG is used, a natural choice

for the graft source site would be the intercondylar

notch because a notchplasty may be performed any-

way—lessening the concern of graft site morbidity. If

the lesion is extensive and ACI is determined as the

most appropriate choice, the procedure will have to be

staged, with the chondrocyte biopsy performed ini-

tially. ACL reconstruction could also be performed at

the time of the initial procedure or 4 to 6 weeks later at

the time of chondrocyte reimplantaton.

ACL surgery with incidental chondral lesion

It is not unusual to find an unexpected chondral

lesion at the time of ACL reconstruction. Patient

preparation and pre-perative discussion is paramount

for success in all cases. Because of the frequent

overlap in symptoms with meniscal pathology, we

inform all arthroscopy patients that there is a like-

lihood that an articular cartilage procedure may be

required at surgery. One must explain the potential

divergence in surgical technique and the postopera-

tive treatment regimen should a cartilage lesion be

identified. Because symptomatology is unknown, the

surgeon should strive to select treatment options that

minimize potential morbidity.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 163

Page 16: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

Chronic ACL with symptomatic chondral lesion

Based on natural history data it is obvious that

ACL deficient knees are prone to developing chon-

dral injury. The incidence of lesion formation

increases as time passes from the initial ligamentous

disruption. A chronically ACL-deficient knee with a

symptomatic chondral lesion requires treatment. As

mentioned before, proper preoperative patient coun-

seling is absolutely essential. If arthoscopy is being

planned on a knee with mechanical symptoms, the

surgeon may not know if the symptoms are caused by

a meniscus tear or a chondral lesion. The expectation

may be that the procedure will be a simple knee

arthroscopy with partial menisectomy, but the patient

needs to be aware that it may be more involved if a

chondral lesion is found and AOG or ACI is selected

for treatment. Because cruciate insufficiency may

jeopardize a healing cartilage graft, cruciate integrity

should be restored to protect a new graft from shear

forces and episodes of instability with either concom-

itant or staged surgery [93,94]. As a general rule,

whenever a chondral lesion in an ACL-deficient knee

is grafted, the ACL should be reconstructed.

An additional and novel graft source for AOG,

unique to chronically ACL-deficient knees, has been

described by Bobic et al as the ‘‘chondro-osteophyte’’

often found on the lateral aspect of the medial

femoral notch [3].

Reconstructed ACL with new lesion

Apatient with a previously reconstructed ACLmay

present with a new symptomatic chondral lesion. This

may be a result of new injury or possibly late sequelae

from the initial injury. The natural history of bone

bruises and their possible role in late chondral lesions

is unclear. In any case, this requires treatment. First of

all, it is critical to assess and ensure integrity of the

ACL graft prior to treating a cartilage lesion because

cruciate integrity must be restored to protect a new

graft from shear forces and episodes of instability.

Assessing the functional status of a reconstructed

ACL can be a challenge, though. Clinical history is

helpful in raising suspicion of a disrupted graft if

there has been an acute reinjury. Physical examina-

tion is helpful, but a knee with a functioning ACL

graft can still exhibit increased anterior translation on

the Lachman test and a positive pivot shift test. MR

image scanning can be helpful but does not provide

functional information about a reconstructed liga-

ment. Instrumented testing of knee laxity, on the

other hand, such as the KT-1000 can reveal functional

information and play a role. Normally, testing is

performed on both knees and the side-to-side differ-

ence in manual maximum anterior translation of the

tibia is compared with the knee at 30� of flexion.

ACL disruption is likely when there is greater than a

3-mm difference. This has been described for acute

tears. Using this technique for evaluating ACL recon-

struction grafts may not be as reliable because a

certain amount of increased laxity is commonly noted

when compared with the normal knee despite a well-

functioning graft. If post-reconstruction baseline val-

ues are available, however, a significant increase in

same-side values may suggest graft rupture. Finally,

direct probing of the ACL graft during a diagnostic

arthroscopy can also provide helpful information.

If AOG is performed, it is important to be aware

that the intercondylar notch may not be available as a

graft source if a notchplasty was performed during

the initial procedure. This is an important considera-

tion because availability of graft material will deter-

mine the maximum-size lesion that can be treated

with this technique. For ACI, an initial arthroscopic

cartilage biopsy would precede concurrent ACL

reconstruction/ACI by 4 to 6 weeks. Rehabilitation

would proceed as it would for an isolated ACI

procedure as outlined above.

Summary

The treatment of articular cartilage lesions remains

one of the great challenges facing orthopedic surgeons

today. The technique of chondrocyte transplantation

has opened the door for the application of biologic

solutions to difficult problems. These techniques will

prove the keystone of further advances into biologic

joint repair and replacement. Enthusiasm, however,

must be tempered by the numerous gaps in cartilage

science and the overwhelming need for further long-

term data to demonstrate the efficacy of these tech-

niques in thwarting the presumed eventual progression

of these lesions toward osteoarthritis. The status of the

articular cartilage is of paramount importance in ACL

decision-making. Every effort must be made to protect

the existing hyaline articular cartilage during ACL

reconstruction. Though current cartilage repair tech-

niques are in their infancy, they remain stepping-

stones to future developments. It is hoped that we will

one day be able to regenerate normal hyaline cartilage

without great morbidity. At present, the ACL surgeon

must accept techniques that diminish symptoms and

do not burn bridges to future advances. The orthopedic

surgeon must increase his knowledge of the basic

science of articular cartilage in order to best choose

from the various cartilage treatments that evolve.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167164

Page 17: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

References

[1] Curl WW, Krome J, Gordon ES, Rushing J, Stat M,

Smith BP, et al. Cartilage injuries: a review of 31,516

knee arthroscopies. Arthroscopy 1997;13(4):456–60.

[2] Browne JE, Branch TP. Surgical alternatives for treat-

ment of articular cartilage lesions. J Am Acad Orth

Surg 2000;8:180–9.

[3] Bobic V. The outcome of accelerated rehabilitation of

ACL reconstructed knees. Presented at Proceedings of

the 2nd World Congress on Sports Trauma and the

22nd AOSSM Annual Meeting, June 1, 1996. Orlando,

FL, 1996.

[4] Barry M, Thomas R, Rees A, et al. Effect of ACL

reconstruction on meniscal and chondral lesions in

the chronic anterior cruciate deficient knee. Knee

1995;2:201–5.

[5] Bradley J, Dandy DJ. Osteochondritis dessicans and

other lesions of the femoral condyles. J Bone Joint

Surg Br 1989;71:518–22.

[6] Zamber RW, Teitz CC, McGuire DA, Frost JD, Her-

manson BK. Articular cartilage lesions of the knee.

Arthroscopy 1989;5(4):258–68.

[7] Buckwalter JA, Mow VC, Ratcliffe A. Restoration of

injured or degenerated articular cartilage. J Amer Acad

Orthop Surg 1994;2(4):192–201.

[8] Takahashi S, Urist MR. Differentiation of cartilage on

three substrata under the influence of an aggregate of

morphogenetic protein and other bone tissue noncol-

lagenous proteins. Clin Orthop 1986;207:227–38.

[9] Mankin HJ, Mow VC, Buckwalter JA, Iannotti JP,

Ratcliffe A. Form and function of articular cartilage.

In: Simon SR, editor. Orthpaedic Basic Science. Rose-

mont, IL: AAOS; 1994. p. 1–44.

[10] Mow VC, Ratcliffe A. Structure and function of artic-

ular cartilage and meniscus. In: Mow VC, Hayes WC,

editors. Basic orthpaedic biomechanics. Philedelphia:

Lippencott-Raven; 1997. p. 113–77.

[11] Buckwalter JA, Hunziker EB. Articular cartilage biol-

ogy and morphology. In: Mow VC, Ratcliffe A, edi-

tors. Structure and function of articular cartilage. Boca

Raton (FL): CRC Press; 1993. p. 318–24.

[12] McDermott AG, Langer F, Pritzker KP, et al. Fresh

small-fragment osteochondral allografts: long-term fol-

low-up study on first 100 cases. Clin Orthop 1985;197:

96–102.

[13] Ateshian GA, Lai WM, ZhuWB, Mow VC. An asymp-

totic solution for the contact of two biphasic cartilage

layers. J Biomechanics 1994;27(11):1347–60.

[14] Borrelli Jr J, Torzilla PA, Grigiene R, Helfet DL. Effect

of impact load on articular cartilage: development of an

intra-articular fracture model. J Orthop Trauma 1997;

11(5):319–26.

[15] Tomatsu T, Imai N, Takewuchi N, Takahashi K, Ki-

mura N. Experimentally produced fractures of aticular

cartilage and bone. J Bone Joint Surg (Br) 1992;

74B(3):457–62.

[16] Vener MJ, Thompson RC, Lewis JL, Oegema Jr TR.

Subchondral damage after transarticular loading: an in

vitro model of joint injury. J Orthop Research 1992;

10(6):759–65.

[17] Vellet AD, Marks PH, Fowler PJ, Munro TG. Occult

post-traumatic osteochondral lesions off the knee:

prevalence, classification, and short-term sequelae

evaluated with MR imaging. Radiology 1991;178:

271–6.

[18] Levy AS, Lohnes J, Sculley S, LeCroy M, Garrett W.

Chondral delamination of the knee in soccer players.

Am J Sports Med 1996;24(5):634–9.

[19] Hunter W. On the structure and diseases of articu-

lating cartilages. Philos Trans Roy Soc 1997;42(B):

514–21.

[20] Terry GC, Flandry F, Van Mansen JW, Norwood LA.

Isolated chondral fractures of the knee. Clin Orthop

1988;234:170–7.

[21] Radin EL, Parker HG, Pugh JW, Steinberg RS, Paul

IL, Rose RM. Response of joint to impact loading. III.

Relationship between trabecular microfractures on car-

tilage degeneration. J Biomechanics 1973;6:51–7.

[22] Bennett GA, Baur W. Further studies concerning the

repair of articular cartilage in dog joints. J Bone Joint

Surg 1935;17:141–50.

[23] Bennett GA, Baur W, Maddock SJ. A study of the

repair of articular cartilage and the reaction of normal

joints of adult dogs to surgically created defects of

articular cartilage, ‘‘joint mice,’’ and patellar displace-

ment. Am J Path 1932;8:499–524.

[24] Calandruccio RA, Gilmer WS. Proliferation, regenera-

tion, and repair of articular cartilage of immature ani-

mals. J Bone Joint Surg 1962;44A:431–55.

[25] Campbell CJ. The healing of cartilage defects. Clin

Orthop 1969;64:45–62.

[26] DePalma AF, McKeever CD, Subin SK. Process of

repair of articular cartilage demonstrated by histology

and autoradiography with tritiated thymidine. Clin Or-

thop 1966;48:229–42.

[27] Fuller JA, Ghadially FN. Ultrastructural observations

on surgically produced partial thickness defects in ar-

ticular cartilage. Clin Orthop 1972;86:193–205.

[28] Jackson DW, Jennings LD, Maywood RM, Berger PE.

Magnetic resonance imaging of the knee. Am J Sports

Med 1988;6(1):29–38.

[29] Mankin HJ. Localization of tritiated thymidine in artic-

ular cartilage of rabbits. II. Repair in immature carti-

lage. J Bone Joint Surg 1962;44 A:688–98.

[30] Mankin HJ. Treaction of articular cartilage to injury

an osteoarthritis. Parts 1–2. Engl J Med 1974;291:

1285–92.

[31] Paget J. Healing of cartilage. Clin Orthop 1988;64:7–8.

[32] Mankin HJ. The response of articular cartilage to me-

chanical injury. J Bone Joint Surg 1982;64A:460–6.

[33] Fowler PJ. Bone injuries associated with anterior cruci-

ate ligament disruption. Arthroscopy 1994;10:453–60.

[34] Speer KP, Spritzer CE, Bassett FH, Feagin Jr JA, Gar-

rett Jr WE. Osseous injury associated with acute tears

of the anterior cruciate ligament. Am J Sports Med

1992;20(4):382–9.

[35] Spindler KP, Schils JP, Bergfeld JA, Andrish JT,

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 165

Page 18: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

Weiker GG, Anderson TE, et al. Prospective study of

osseous, articular and meniscal lesions in anterior

cruciate ligament tears by magnetic resonance imag-

ing and arthroscopy. Am J Sports Med 1993;21(4):

551–7.

[36] Stein LN, Fischer DA, Fritts HM, et al. Occult osseous

lesions associated with anterior cruciate ligament tears.

Clin Orthop 1995;313:187–93.

[37] Johnson DL, Urban WP, Caborn DNM, Vanarthos WJ,

Carlson CC. Articular cartilage changes seen with

magnetic resonance imaging-detected bone bruises as-

sociated with acute anterior cruciate ligament rupture.

Am J Sports Med 1998;26:409–14.

[38] Wojtys E, Wilson M, Buckwlater K, Braunstein E,

Martel W. Magnetic resonance imaging of knee hya-

line cartilage and intraarticular pathology. Am J Sports

Med 1987;15(5):455–63.

[39] Gylys-Morin VM, Hajek PC, Sartoris DJ, Resnick D.

Articular cartilage defects: detectability in cadaver

knees with MR. Am J Radiology 1987;148:1153–7.

[40] Burstein D, Bashir A, Gray ML. MRI techniques in

early stages of cartilage disease. Invest Radiol 2000;

35:622–38.

[41] McCauley T, Disler D. Magnetic resonance imaging of

articular cartilage of the knee. J Am Acad Orth Surg

2001;9:2–8.

[42] Baur M, Jackson RW. Chondral lesions of the femoral

condyles: a system of arthroscopic classification. Ar-

throscopy 1988;4(2):97–102.

[43] Dzioba RB. The classification and treatment of acute

articular cartilage lesions. Arthroscopy 1988;4(2):

72–80.

[44] Imai N, Tomatsu T. Cartilage lesions in the knee of

adolescents and young adults: arthoscopic analysis.

Arthoroscopy 1991;7(2):198–203.

[45] Jackson RW. Meniscal and articular cartilage injury in

sport. J R Coll Surg Edinb 1993;34(Suppl):s15–7.

[46] Miller DV, O’Brien SJ, Arnoczky SS, Kelly A, Fealy

SV, Warren RF. The use of the contact Nd:YAG laser

in arthroscopic surgery: effects on articular cartilage

and meniscal tissue. Arthroscopy 1989;5(4):245–53.

[47] Johnson L. Arthroscopic abrasion arthroplasty histori-

cal and pathologic perspective: present status. Arthro-

scopy 1986;2:54–69.

[48] Lu Y, Hayashi K, Hecht P, et al. The effect of monopo-

lar radiofrequency energy on partial-thickness defects

of articular cartilage. Arthroscopy 2000;16:527–36.

[49] Ryan A, Bertone A, Kaeding C. The effects of radio-

frequency treatment on chondrocytes and articular car-

tilage matrix of fibrillated cartilage. Presented at the

ACL Study Group, March 5, 2002. Big Sky, MT.

[50] Kaplan L, Uribe JW. The acute effects of radiofre-

quency energy in articular cartilage: an in vitro study.

Arthroscopy 2000;16:2–5.

[51] Lu Y, Edwards III RB, Kalscheur VL, et al. Effect of

bipolar radiofrequency energy on human articular car-

tilage. Comparison of confocal laser microscopy and

light microscopy. Arthroscopy 2001;17:117–23.

[52] Barber FA, Uribe JW, Weber SC. Current applications

for arthroscopic thermal surgery. Arthroscopy 2002;18:

40–50.

[53] Moller H. Holmium laser versus mechanical cartilage

resection: comparative studies in the rabbit arthrosis

model. Lagenbachs Arch Chir 1994;379:84–94.

[54] Stein DT, Ricciardi CA, Viehe T. The effectiveness of

the use of electrocautery with chondroplasty in treating

chonromalacic lesions: a randomized prospective

study. Arthroscopy 2002;18:190–3.

[55] Gill T, Macgillivray J. The technique of microfracture

for the treatment of articular cartilage defects in the

knee. Op Tech in Orthop 2001;2:105–7.

[56] Ogilvie-Harris DJ, Jackson RW. The arthroscopic treat-

ment of chondromalacia patella. J Bone Joint Surg

1984;66B:660–5.

[57] Rae PJ, Noble J. Arthroscopic drilling of osteochon-

dral lesions of the knee. J Bone Joint Surg 1989;71B:

534–41.

[58] Rodrigo JJ, Steadman RJ, Sillman JF, et al. Improve-

ment of full-thickness chondral defect healing in the

human knee after debridement and microfracture using

continuous passive motion. Am J Knee Surg 1994;7:

109–16.

[59] Schonholtz GJ, Ling B. Arthroscopic chondroplasty of

the patella. Arthroscopy 1985;1:92–6.

[60] Sprague III NF. Arthroscopic debridement for degener-

ative knee joint diseas. Clin Orthop 1981;160:118–23.

[61] Mitchell N, Shepard N. The resurfacing of adult rabbit

articullar cartilage by multiple perforations through

the subchondral bone. J Bone Joint Surg 1976;58A:

230–3.

[62] Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaks-

son O, Peterson L. Treatment of deep cartilage defects

in the knee with autologous chondrocyte transplanta-

tion. N Engl J Med 1994;331(14):889–95.

[63] Genzyme Articular Cartilage Study Group. Bone

bruises on MRI. Presented at AAOS annual meeting,

March 21, 1998. New Orleans, LA: 1998.

[64] Steadman R. Biological resurfacing of large articular

cartilage defects. Presented at AAOS annual meeting,

February 13–16, 1997. Meniscus and Articular Carti-

lage Study Group. San Francisco, CA, 1997.

[65] Steadman JR, Rodkey WG, Singleton SB, Briggs KK.

Microfracture technique for full thickness chondral de-

fects: technique and clinical results. Op Tech in Ortho

1997;7:300–7.

[66] Bert JM. Abrasion arthroplasty. Oper Tech Orthop

1997;7:294–9.

[67] Ogilvie-Harris DJ, Fitsialos DP. Arthroscopic manage-

ment of the degenerative knee. Arthroscopy 1991;7:

151–7.

[68] Nehrer S, Spector M, Minas T. Histologic analysis of

tissue after failed cartilage repair procedures. Clin Or-

thop 1999;365:149–62.

[69] Gill TJ, Steadman JR, Rodrigo JJ, et al. Indications and

long-term clinical results of microfracture. Presented at

the 2nd Symposium of the International Cartilage Re-

pair Society, November 15, 1998. Boston (MA): 1998.

[70] Mayer G, Seidle GC. Chondral and osteochondral frac-

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167166

Page 19: Approach to cartilage injury in the anterior cruciate ligament-deficient knee

tures of the knee joint-treatment and results. Arch Or-

thop Trauma Surg 1988;107:154–7.

[71] Judet H. Essai sur la greffe des tissues articulares.

Comp Rend Acad D Sciences 1908;146:193–6.

[72] Campbell CJ, Grisolia A, Zanconato G. The effects pro-

duced in the cartilaginous epihyseal plate of immature

dogs by experimental surgical traumata. J Bone Joint

Surg 1959;45-A:1221–42.

[73] Pap K, Krompecher S. Arthroplasty of the knee- ex-

perimental and clincial experiences. J Bone Joint Surg

1961;43A:523–37.

[74] Entin MA, Alger JR, Baird RM. Experimental and

clinical transplantation of autogenous whole joints.

J bone Joint Surg 1962;44A:1518–36.

[75] Campbell CJ, Ishida H, Takahashi H, et al. The trans-

plantation of articular cartilage: an experimental study

in dogs. J Bone Joint Surg 1963;45A:1579–92.

[76] Pelker RR, Friedlaender GE. Boimechanical consider-

ations in osteochondral grafts. In: Friedlaender GE,

Goldberg VM, editors. Bone and cartilage allografts.

Rosemont (IL): American Acadamy of Orthpaedic Sur-

geons; 1991. p. 155–62.

[77] Hangody L, Karpati Z. A new surgical treatment of

localized cartilagenous defects of the knee. Hungarian

Journal of Orthopaedic Trauma 1994;37:237–42.

[78] Levy A. Osteochondral autograft for the treatment of

focal cartilage lesions. Op Tech in Ortho 2001;11(2):

108–14.

[79] Bobic V. Arthroscopic osteochondral autograft trans-

plantation in anterior cruciate ligament reconstruction:

a preliminary clinical study. Knee Surg, Sports Trau-

matol, Arthroscopy 1996;3:262–4.

[80] Simonian PT, Sussman PS, Wickiewicz TL, et al. Con-

tact pressures at osteochondral donor sites in the knee.

Am J Sports Med 1998;26:491–4.

[81] Manlin TI, Mnaymneh W, Lo HF. Cryopreservation of

articular cartilage. Ultrastructural observations and

long term results of experimental distal femoral trans-

plantation. Clin Orthop 1994;303:18–32.

[82] Sammarco VJ, Gorab R, Miller R, Brooks P. Human

articular cartilage storage in cell culture medium:

guidelines for storage of fresh osteochondral allografts.

Orthopedics 1997;20:497–500.

[83] Tomford W, Mankin H. Investigational approaches to

articular cartilage preservation. Clin Orthop 1983;

174:22–7.

[84] Langer F, Gross AE. Immunogenicity of allograft

articular cartilage. J Bone Joint Surg 1974;56A:

297–304.

[85] Sgaglione NA, Miniaci A, Gillogly SD, Carter TR.

Update on advanced surgical techniques in the treat-

ment of traumatic focal articular cartilage lesions of the

knee. Arthroscopy 2002;18:9–32.

[86] Mankin HJ, Fogelson FS, Thrasher AZ, et al. Massive

resection and allograft transplantation in the treatment

of malignant bone tumors. N Engl J Med 1976;294:

1247–55.

[87] Delaney- JP, O’Driscoll SW, Salter RB. Neochondro-

genesis in free intra-articular periosteal autografts in

an immobilized and paralyzed limb. An experimental

investigation in the rabbit. Clin Orthop 1989;248:

278–82.

[88] O’Driscoll S, Kelley FW, Salter RB. Durability of re-

generated articular cartilage produced by free autoge-

nous periosteal grafts in major full-thickness defects in

joint surfaces under the influence of continuous pas-

sive motion. A follow-up report at one year. J Bone

Joint Surg 1988;70A:595–606.

[89] O’Driscoll S, Salter R, Kelley F. The chondrogenic

potential of free autogenous periosteal grafts for bio-

logical resurfacing of major full-thickness defects in

joint surfaces under the influence of continuous pas-

sive motion: an experimental investigation in the rab-

bit. J Bone Joint Surg 1988;68A:1017–35.

[90] O’Driscoll S. Autologous chondrocyte implantation.

Presented at the AAOS annual meeting, December

14, 1997. San Francisco, CA, 1997.

[91] Shapiro F, Koide S, Glimcher MJ. Cell origin and

differentiation in the repair of full-thickness defects

of articular cartilage. J Bone Joint Surg 1993;75-A:

532–53.

[92] Anderson AF. Cartilage repair registry summary re-

port. Presented at the AAOS annual meeting, February

15, 2002. Dallas, TX.

[93] Cole BJ, D’Amato M. Autologous chondrocyte im-

plantation. In: Fu F, editor. Operative techniques in or-

thopaedics, Vol. 11. Philadelphia: WB Saunders; 2001.

p. 115–31.

[94] Minas T, Peterson L. Autologous chondrocyte trans-

plantation. In: Drez D, DeLee JC, editors. Operative

techniques in sports medicine, vol. 8. 2000. p. 144–57.

A.S. Levy, S.W. Meier / Orthop Clin N Am 34 (2003) 149–167 167