Upper limb Osteochondral autologous transplantation for the

Upper limb
Osteochondral autologous transplantation
for the treatment of full-thickness articular
cartilage defects of the shoulder
M. Scheibel,
C. Bartl,
P. Magosch,
S. Lichtenberg,
P. Habermeyer
From ATOS-Clinic
Heidelberg,
Heidelberg, Germany
M. Scheibel, MD, Resident
C. Bartl, MD, Resident
P. Magosch, MD, Resident
S. Lichtenberg, MD, Chief
of the Department
P. Habermeyer, MD, Chief
of the Department
Department of Shoulder and
Elbow Surgery, ATOS-Clinic
Heidelberg, Bismarckplatz 915, 69115 Heidelberg,
Germany.
Correspondence should be
sent to Dr M. Scheibel.
©2004 British Editorial
Society of Bone and
Joint Surgery
doi:10.1302/0301-620X.86B7.
14941 $2.00
J Bone Joint Surg [Br]
2004;86-B:991-7.
Received 9 October 2003;
Accepted after revision
9 December 2003
We performed eight osteochondral autologous transplantations from the knee joint to the
shoulder. All patients (six men, two women; mean age 43.1 years) were documented
prospectively. In each patient the stage of the osteochondral lesion was Outerbridge grade
IV with a mean size of the affected area of 150 mm2. All patients were assessed by using the
Constant score for the shoulder and the Lysholm score for the knee. Standard radiographs,
magnetic resonance imaging and second-look arthroscopy were used to assess the
presence of glenohumeral osteoarthritis and the integrity of the grafts. After a mean of 32.6
months (8 to 47), the mean Constant score increased significantly. Magnetic resonance
imaging revealed good osseointegration of the osteochondral plugs and congruent
articular cartilage at the transplantation site in all but one patient. Second-look arthroscopy
performed in two cases revealed a macroscopically good integration of the autograft with
an intact articular surface.
Osteochondral autologous transplantation in the shoulder appears to offer good clinical
results for treating full-thickness osteochondral lesions of the glenohumeral joint. However,
our study suggests that the development of osteoarthritis and the progression of preexisting osteoarthritic changes cannot be altered by this technique.
The spontaneous capacity for repair of damaged articular cartilage is limited.1-4 Arthroscopic lavage, shaving or debridement provide
only temporary relief of symptoms and do not
stimulate the regeneration of the chondral
lesion.5-7 In addition, a recently published,
double-blinded, randomised, placebo-controlled trial has shown that arthroscopic lavage
and debridement is no better than a placebo
procedure.8 Bone marrow stimulation techniques such as subchondral drilling, microfracture and abrasion arthroplasty create a
fibrocartilage or hyaline-like cartilage cover
that provides less mechanical stability against
tear and shear forces.9-11
Transplantation of osteochondral autografts
has become a popular and widely accepted
technique for treating circumscribed osteochondral lesions. Most clinical studies have
concentrated upon the treatment of focal cartilage defects of the knee and ankle joints.12-20
Focal osteochondral lesions of the shoulder are
less common than those of the lower extremities. However, they are often symptomatic and,
if left untreated, fail to heal and may progress
to glenohumeral osteoarthritis. After the
encouraging results of osteochondral autologous transplantation in the knee and ankle
VOL. 86-B, No. 7, SEPTEMBER 2004
joints we have started to use the osteochondral
autologous transfer system (OATS) on patients
with full-thickness osteochondral lesions of the
shoulder. Our aim was to evaluate the clinical
and radiological results of the procedure, as
well as its risks.
Patients and Methods
In a retrospective study we assessed the clinical
and radiological results of eight osteochondral
autologous transplantations from the knee to
the shoulder. The diagnosis was established by
history, clinical examination, standard radiographs, magnetic resonance imaging and diagnostic arthroscopy.
Inclusion criteria for this study were patients
with circumscribed, Outerbridge grade IV,21
osteochondral lesions of the humeral head or
the glenoid, an affected area greater than 100
mm2, and no or mild osteoarthritic changes
(≤ stage I according to Samilson and Prieto22).
Patients with superficial chondral lesions (Outerbridge grades I to III),21 lesions greater than
250 mm2 and advanced radiological signs of
glenohumeral osteoarthritis (≥ stage II according to Samilson and Prieto22) were excluded.
All patients were informed about the unknown
natural course of the osteochondral lesion, the
991
992
M. SCHEIBEL, C. BARTL, P. MAGOSCH, S. LICHTENBERG, P. HABERMEYER
Table I. Characteristics of the patients, defects and procedures
Patient
Gender
Age
(yrs)
1
M
57
2
M
38
3
4
M
M
56
53
5
F
43
6
7
M
M
44
23
8
F
31
Aetiology
Location*
Size of defect Number of
cylinders used
(mm2)
Traumatic anterior
instability
Traumatic anterior
instability
Post-traumatic
Hyperlaxity
Central (h)
120
1
Posteromedial (h)
150
3
Central (h)
Posterocentral (h)
105
105
2
2
Anterocentral (g)
128
1
Central (h)
Anterocentral (h)
144
250
1
3
Posteromedial (h)
200
2
Traumatic anterior
instability
Hyperlaxity
Traumatic posterior
subluxation
Traumatic anterior
instability
Additional
procedures
performed
Labral augmentation, capsular shift
None
None
Labral augmentation, capsular shift
Labral augmentation, capsular shift
None
None
Labral augmentation, capsular shift
* h, humeral; g, glenoid
documented clinical and radiological results of the osteochondral transplantation procedure in the knee and ankle
joints, as well as the surgical technique and alternative therapeutic options.
Pre- and post-operatively the clinical evaluation included
the Constant score for the shoulder and the Lysholm score
for the knee joint.23,24 Patients were reviewed at six weeks,
six months and one year post-operatively and at the most
recent follow-up. The final assessment was performed by an
independent examiner and not by the surgeon. Standard
radiographs (true anteroposterior, true anteroposterior in
external and internal rotation and axillary views) were used
to assess the presence of glenohumeral osteoarthritis. Signs
of glenohumeral osteoarthritis were graded according to
the classification of Samilson and Prieto.22 MRI was performed post-operatively in every patient in order to assess
the integrity of the osteochondral grafts. As osteochondral
autologous transplantation has not been fully investigated
in the shoulder, a second-look arthroscopy six months postoperatively was recommended to all patients, but performed in only two. The remaining patients refused further
surgical intervention.
Statistical analysis between variables pre- and post-operatively was performed with the Wilcoxon signed-rank test
for non-parametric data. The level of significance was set at
p < 0.05. The statistical software used was StatView (Abacus Concepts Inc, Berkeley, California).
Operative technique. All procedures were performed in the
beach chair position under interscalene block and general
anaesthesia. A diagnostic glenohumeral arthroscopy was
performed using a standard posterior portal. According to
the International Cartilage Repair Society the defect was
classified on the basis of its location, size, thickness and the
condition of the opposing articular surface. In each patient
Fig. 1a
Fig. 1b
Intra-operative findings. A grade IV osteochondral lesion of the humeral head a) before and b) after autologous transplantation with two osteochondral
plugs.
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OSTEOCHONDRAL AUTOLOGOUS TRANSPLANTATION
993
Table II. Clinical results
Constant score (pre-operatively)
Constant score (post-operatively)
Patient
Pain
ADL*
ROM†
Follow-up
Strength
(kg)
Total (mths)
1
2
3
4
5
6
7
8
10
10
5
13
12
5
10
5
9
12
10
16
17
14
18
7
38
40
38
30
40
40
40
40
9.7
9.9
8.4
5.0
4.5
3.3
10.4
2.7
77.2
82.6
70.5
69.4
78.4
65.9
89.6
57.6
36
41
47
44
30
24
31
8
Lysholm score
Pain
ADL
ROM
Strength
(kg)
Total Total
15
13
13
15
15
15
15
15
20
18
19
18
20
20
20
18
36
40
40
36
40
40
40
40
10.6
11.1
6.9
6.9
6.0
6.1
9.9
4.7
93.1
94.1
86.3
83.4
87.5
87.7
95.4
82.4
100
100
91
100
100
100
87
64
* ADL, activities of daily living
† ROM, range of movement
the stage of the osteochondral lesion was Outerbridge
grade IV with a mean size of 150 mm2 (105 to 250 mm2). In
seven patients the defect was located on the humeral side
and in one patient it was on the glenoid side. In three
patients the defect was central in position, in three it was
posteromedial and in one it was posterocentral on the
humeral head. The one glenoid defect was positioned
anteromedially (Table I).
The transplantation procedure was performed with an
osteochondral autograft transfer system (Arthrex, Naples,
Florida). The shoulder joint was exposed through a standard deltopectoral approach and the cephalic vein was preserved and retracted laterally. The subscapularis muscle
was detached from the lesser tuberosity approximately 0.5
cm from its insertion, and stay sutures were attached for
subsequent refixation and the muscle was then retracted
medially. If capsular instability was present the subscapularis was stripped from the anterior capsule in order to perform a capsular shift at the end of the procedure. The
humeral head was next exposed and the defect was
inspected (Fig. 1a). The size of the lesion was again measured using a range of appropriate colour-coded sizers. A
recipient socket was then created in order to provide an
adequate press-fit graft fixation. The appropriately sized
tubular harvester was introduced into the joint and placed
over the affected area, taking great care to ensure that the
harvester was perpendicular to the articular surface. The
decision to transplant single or multiple osteochondral
grafts was based upon the size and location of the defect.
Either one (three patients), two (three patients), or three
(two patients) osteochondral plugs were used in order to fill
the defects (Table I). Next, the osteochondral graft was
taken. The knee joint was exposed through a lateral miniarthrotomy. The chosen donor site was in an area along the
outer edge of the lateral femoral condyle, immediately
above the sulcus terminalis. This is a low weight-bearing
area and offers a convex articular surface similar to that of
the central humeral head.25 The tube harvester was inserted
into the joint and placed perpendicular to the selected harvest site. It was then driven into the bone to the same depth
as the osteochondral defect and the graft was harvested.
The donor cavities were not filled. The harvested grafts
VOL. 86-B, No. 7, SEPTEMBER 2004
were then transferred into the prepared recipient site using
a press-fit technique (Fig. 1b).
In order to address any underlying instability or capsular
redundancy an additional labral augmentation (Harryman
et al26) and a lateral capsular shift (Matsen et al27) was performed in four patients. Finally, the subscapularis tendon
was reattached anatomically with the arm in 30˚ of abduction and 20˚ of external rotation.
Post-operative management. Post-operatively, the patients
underwent a standard rehabilitation programme. The
affected arm was placed in an abduction pillow for three
weeks. Passive range of movement was initiated on the
third post-operative day and was restricted to 60˚ of flexion, abduction and internal rotation for the first two weeks
and then increased to 90˚ up to the five-week point. External rotation was prohibited up to the six-week point in
order to protect the reconstructed anterior capsule and subscapularis tendon. Four to six weeks post-operatively the
patient started active movements and a muscle strengthening programme.
Results
The mean age of the patients was 43.1 years (23 to 57). The
dominant shoulder was affected in six patients. Full details
are summarised in Table I.
Clinical. Seven patients were available for medium term
follow-up and one for short-term follow-up (Table II).
After a mean follow-up of 32.6 months (8 to 47) the overall
Constant score improved significantly from 73.9 points (57
to 89.6) to 88.7 points (82.4 to 95.4) (p < 0.05). All patients
had less pain when compared with their original pre-operative rating. There was a significant (p < 0.05) increase in
the overall pain rating scale from the initial mean score of
8.7 (5 to 13) to the latest follow-up score of 14.5 (13 to 15).
Six patients were completely free of pain. The mean activities of daily living (ADL) rate increased significantly
(p < 0.05) from 12.9 (7 to 18) to 19.1 (18 to 20). All but
two patients achieved their full work and sporting activity
levels. The results for range of movement and strength also
increased although these were not statistically significant
(p > 0.05 for both) and probably due to pain relief. The
functional outcome of the knee was graded with the
994
M. SCHEIBEL, C. BARTL, P. MAGOSCH, S. LICHTENBERG, P. HABERMEYER
Fig. 2a
Fig. 2b
Anteroposterior radiograph of a shoulder a) before and b) 24 months after autologous osteochondral transplantation. Note the increase in inferior osteophyte formation between the pre- and post-operative examinations.
Lysholm score.24 Six patients had an excellent result (91 to
100 points), one patient had a satisfactory result (77 to 90
points) and one patient had a poor result (0 to 76 points).
Full clinical results are shown in Table II.
Radiographic. Pre-operatively, four patients had stage I
glenohumeral osteoarthritic changes.22 In all but one the
osteoarthritis had deteriorated between the pre- and postoperative assessments. The patient who did not progress
was only available for short-term follow-up. Four patients
did not show any signs of glenohumeral osteoarthritis preoperatively (Fig. 2a). However, by their latest follow-up all
four had developed new inferior humeral osteophyte formation (Fig. 2b) although this did not influence the final
clinical result. Despite an increase in the size of humeral
osteophytes the mean glenohumeral distance did not significantly reduce between the pre-operative (4.4 mm) and
post-operative (4.2 mm) examinations (p > 0.05).
MRI, which was performed in the paracoronal, transaxial and parasagittal planes, revealed excellent graft viability and congruence of the chondral surfaces (Fig. 3) in all
but one patient. In one patient, signs of transplant insufficiency with evidence of avascular necrosis could be seen.
However the patient was clinically asymptomatic and satisfied with the post-operative result. Full radiographic results
are shown in Table III.
Second-look arthroscopy. In two patients a second-look
arthroscopy (Table III) was performed six months postoperatively in order to assess the chondral surfaces. In both
there was good macroscopic integration of the grafts with
Fig. 3
Post-operative paracoronal MRI, 24 months after autologous osteochondral transplantation showing an
intact osteochondral plug and a congruent articular
surface.
the original osteochondral defect being completely covered
by chondral tissue (Fig. 4). The surrounding chondral surface showed some superficial fissuring, representing a grade
I chondral lesion according to Outerbridge.21
Complications. No complications which could be directly
related to the surgical procedure in the shoulder were seen.
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995
Table III. Staging, radiographic, MRI and arthroscopic results
Stage of osteoarthritis18
Glenohumeral distance (mm)
Patient
Pre-operative
Post-operative Pre-operative
Graft integrity on
Post-operative MRI
Graft integrity at second-look
arthroscopy
1
2
3
4
5
6
7
8
I
I
None
None
None
I
None
I
II
II
III
II
I
II
I
I
5
4
4
3
5
3
5
5
Congruent surface
Not performed
Not performed
Not performed
Not performed
Not performed
Congruent surface
Not performed
5
4
4
4
5
3
5
5
However, one patient reported persistent pain and recurrent effusions of the donor knee. This patient achieved a
poor Lysholm score result (< 75 points) by their latest
follow-up. Because of donor site morbidity the patient
underwent two revision arthroscopic surgical procedures
with debridement of the knee joint. Although the shoulder
was completely painless eight months post-operatively the
patient was dissatisfied with the procedure and was
unavailable for medium-term follow-up.
Intact
Intact
Intact
Avascular necrosis
Intact
Intact
Intact
Intact
Osteochondral lesions of the shoulder are less common
than those of the lower extremity but can cause considerable symptoms. These might include joint pain, effusion and
mechanical dysfunction. Although the natural history of
isolated osteochondral defects has not been well defined,
clinical experience has shown that these lesions may
progress to symptomatic degeneration of the joint. Consequently, the treatment of selected, isolated, articular cartilage lesions may delay or prevent the development of
osteoarthritis.
The aim of all methods of articular cartilage restoration
is to reproduce the mechanical, structural and biochemical
properties of the original hyaline articular surface.
Although different studies have reported good and excellent clinical results from autologous chondrocyte implantation (ACI), osteochondral autograft transplantation is
currently the only technique that appears to maintain the
characteristics of hyaline cartilage.15,16,28-30 Bobic13 stated
that the main reason for the long-term survival of transplanted hyaline cartilage was the preservation of an intact
tidemark and cancellous bone barrier. Transplantation of
articular cartilage as a part of an osteochondral graft has
been shown to be an effective method of replacing focal
areas of damaged articular cartilage and reducing pain in
both the knee and ankle joints.12-20
Our study shows that osteochondral transplantation
from the knee to the shoulder results in a good clinical outcome in terms of pain relief and functional recovery. We
observed a significant increase in the overall Constant score
between the pre- and post-operative assessments. At their
latest follow-up, all but two of our patients were com-
Fig. 4a
Fig. 4b
Discussion
Arthroscopic view of a grade IV osteochondral lesion a) before and b) six months after autologous transplantation.
VOL. 86-B, No. 7, SEPTEMBER 2004
996
M. SCHEIBEL, C. BARTL, P. MAGOSCH, S. LICHTENBERG, P. HABERMEYER
pletely pain-free and able to perform all activities of daily
living. Two patients had even returned to overhead sports
activities. It is important to understand that the functional
results which our patients obtained are not only due to the
osteochondral transplantation procedure but also to the
correction of the underlying and additional glenohumeral
pathology. In four patients with recurrent instability of the
shoulder a capsular shift with labral augmentation was performed.
It is significant that in all of our patients glenohumeral
osteoarthritic changes were present at their latest followup. Although the glenohumeral distance on the anteroposterior radiograph did not change significantly, inferior
osteophyte formation was seen in all patients. For those
who had stage I osteoarthritis pre-operatively, all but one
showed a significant deterioration between the pre- and
post-operative assessments although this was never by
more than one stage. The one patient who did not progress
was only available for short-term follow-up. Four patients
had no signs of glenohumeral osteoarthritis pre-operatively.
However, by their latest follow-up all had developed new,
inferior humeral osteophyte formation. Despite this, these
osteoarthritic changes did not correlate with either postoperative pain or the final post-operative result. This
progression in glenohumeral osteoarthritis still poses the
question as to whether osteochondral transplantation may
slow down the development of symptomatic glenohumeral
osteoarthritis at all. In all but one patient MRI follow-up
revealed excellent graft viability and congruence of the
chondral surfaces. In one patient there were signs of graft
insufficiency, probably due to avascular necrosis. However,
this patient was pain-free and very satisfied with the result.
The potential disadvantages of this technique include
donor site morbidity, a limited supply of grafts, dead space
between circular grafts, graft integration and the different
mechanical properties and geometry between donor and
recipient hyaline cartilage.2-4 Donor site morbidity is perhaps the most important risk factor when performing an
osteochondral transplantation from the knee to the shoulder. Studies have shown that donor sites normally refill with
cancellous bone and fibrocartilage and do not cause significant problems.13,19,31 However, persistent pain and recurrent effusions of the donor knee were seen in one of our
patients. Although the shoulder was pain-free the patient
required two revision arthroscopic procedures. Donor site
morbidity can clearly be a serious problem and must be
taken into consideration when counselling a patient for
an osteochondral transplantation from the knee to the
shoulder.
The ideal osteochondral defect for an osteochondral
autologous transplantation in the shoulder is relatively
small, perhaps 10 to 20 mm in diameter.13 In our study
group the mean size of the affected area was 150 mm2 (105
to 250). Large osteochondral defects are not suitable for
this technique as osteochondral grafts are limited and it is
also technically difficult to reconstruct a large subchondral
defect. A large number of grafts may also lead to instability
in the transplantation area. Other problems with this
technique are differences in the thickness, biomechanical
composition and mechanical properties of the articular
cartilage of the knee joint when compared with the
shoulder.
Although we experienced no difficulties in performing
this procedure, the final clinical results may be very
technique-dependent. There are many peri-operative pitfalls that need to be considered. In particular, an appropriate length of graft is essential to a successful outcome. If too
long or too short, an osteochondral cylinder can lead to
incongruity of the articular surface. Also, if the graft is not
inserted in an orthograde fashion an adequate press-fit
cannot be achieved which may lead to loosening or failed
integration.
Our study has certain limitations. It includes only a small
number of patients so that statistical analysis is restricted.
Despite this, to our knowledge it is the first study to document the medium-term clinical and radiographic results for
patients with full-thickness cartilage lesions of the shoulder
who have been treated by osteochondral autologous transplantation. It must also be remembered that not all of the
patients had the same aetiology for their osteochondral
defect. Finally, in three patients the associated underlying
pathology was also corrected which must be taken into
account when interpreting the clinical results.
In summary, osteochondral autologous transplantation
in the shoulder appears to offer good clinical results for the
treatment of osteochondral lesions of the glenohumeral
joint. However, the results of our study suggest that the
development of osteoarthritis and the progression of preexisting osteoarthritic changes cannot be altered by the
technique.
No benefits in any form have been received or will be received from a commercial party related directly to the subject of this article.
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