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Results after microfracture of full-thickness chondral defects in different compartments in the knee
OsteoArthritis and Cartilage (2006) 14, 1119e1125 ª 2006 Published by Elsevier Ltd on behalf of OsteoArthritis Research Society International. doi:10.1016/j.joca.2006.05.003
International Cartilage Repair Society
Results after microfracture of full-thickness chondral defects in different compartments in the knee P. C. Kreuz M.D.y*, M. R. Steinwachs Ph.D.y, C. Erggelet Ph.D.y, S. J. Krausey, G. Konrad M.D.y, M. Uhl M.D.z and N. Su¨dkamp Ph.D.y y Department of Orthopaedic and Trauma Surgery, Albert Ludwig University Freiburg, Hugstetterstrasse 55, 79106 Freiburg, Germany z Department of Radiology, Albert Ludwig University Freiburg, Hugstetterstrasse 55, 79106 Freiburg, Germany Summary Objective: To determine if the clinical results after microfracture of full-thickness cartilage lesions deteriorate over a period of 36 months. Methods: Between 1999 and 2002 85 patients (mean age 39.5 years) with full-thickness cartilage lesions underwent the microfracture procedure and were evaluated preoperatively and 6, 18 and 36 months after surgery. Exclusion criteria were meniscal pathologies, axial malpositioning and ligament instabilities. Baseline clinical scores were compared with follow-up data by paired Wilcoxon-tests for the modified Cincinnati knee and the International Cartilage Repair Society (ICRS)-score. The effects of the lesion localization and Magnetic resonance imaging (MRI) parameters were evaluated using the Pearson correlation and independent samples tests. Results: Both scores revealed significant improvement 18 months after microfracture (P < 0.0001). Within the second 18 months after surgery there was a significant deterioration in the ICRS-score (P < 0.0001). The best results could be observed in chondral lesions of the femoral condyles. Defects in other areas of the knee deteriorated between 18 and 36 months after microfracture. MRI 36 months after surgery revealed best defect filling in lesions on the femoral condyles with significant difference in the other areas (P < 0.02). The Pearson coefficient of correlation between defect filling and ICRS-score was 0.84 and significant at the 0.01 level. Conclusions: Microfracture is a minimal invasive method with good short-term results in the treatment of small cartilage defects. A deterioration of the results starts 18 months after surgery and is most evident in the ICRS-score. The best prognostic factors have young patients with defects on the femoral condyles. ª 2006 Published by Elsevier Ltd on behalf of OsteoArthritis Research Society International. Key words: Osteoarthritis, Marrow stimulation technique, Microfracture, Cartilage lesion.
but partially preserved between the microfracture holes improving load-bearing characteristics following healing3. In contrast to Pridie drilling no heat necrosis or polishing is introduced into the subchondral bone and marrow with microfracture4,5. The equipment is standardized and the costs are minimal since expensive cell cultures are not necessary. Unlike osteochondral, perichondral, periosteal or chondral autograft procedures the problem of a harvest site morbidity is excluded6. The intervention leads to a spontaneous repair response, which is based upon therapeutically induced bleeding from the opened subchondral bone spaces and subsequent blood-clot formation7. Knutsen has compared in a recent study the histological results after microfracture and autologous chondrocyte implantation (ACI). The predominant repair tissue after microfracture was fibrocartilage. For the small number of biopsies and the short-term follow-up of 2 years there was no significant difference in the histological results after ACI8,9. Furthermore animal studies have shown that the tissue formed after microfracture is fibrous in nature10 and not durable11,12. Therefore a long-term cure cannot be expected from the performance of this marrow stimulation technique. Regardless of these poor biomechanical prerequisites recent studies with long-term follow-up over 10 years
Introduction Microfracture is one of many methods available to treat articular cartilage lesions. The technique has been elaborated by Steadman et al. and applied chiefly in young athletes and in young patients generally1,2. There are some inherent advantages. The microfracture technique is minimally invasive because it is arthroscopic through standard portals in most cases. In comparison to an abrasion chondroplasty the subchondral bone plate is not completely destructed 1
Parts of the study were presented at the nineteenth and twentyfirst annual congress of the International Society for Orthopaedics Traumatology and Sports Medicine, Munich, Germany, June 2004 and May 2006 at the first common annual congress for orthopaedic and trauma surgery, Berlin, Germany, October 2005, and at the sixth ICRS-symposium (International Cartilage Repair Society) in San Diego, USA, January 2006. No support in form of grants, equipment or other items has occurred for this project. *Address correspondence and reprint requests to: Peter Cornelius Kreuz, M.D., Department of Orthopaedic Surgery, Albert Ludwig University of Freiburg, Hugstetterstrasse 55, 79106 Freiburg, Germany. Tel: 49-761-270-2401; Fax: 49-761-270-2619; E-mail: [email protected] Received 21 June 2005; revision accepted 9 May 2006.
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have shown improvement in function without significant deterioration over the time. However these studies are only functional outcome case series of patients with chondral lesions, based on special self-administered questionnaires sent to the patients after surgical intervention4. There is only one prospective study with a 2-year followup and a serial objective observation by clinical and histological evaluation9. The present prospective study is based on scores with a continuous objective patient evaluation including control MRI’s over a period of 36 months.
Patients and methods
within the previous month or knee arthroscopy within the previous 6 months. STUDY DESIGN
The prospective study with a 36-months follow-up was conducted to determine the efficacy of microfracture in the postoperative follow-up. Furthermore we wished to figure out if primary good results 6 or 12 months after surgery remain on the same level or deteriorate after a period of 36 months. STUDY COURSE
Between 1999 and 2002 a total of 85 patients with fullthickness chondral defects of the knee underwent the microfracture procedure. Thereof 70 patients (33 males, 37 females) with an average age of 39.5 years (range 19e55 years) met the inclusion criteria (below). Depending on the localization of the defects (femoral condyles, trochlea, tibia or retropatellar) the patients were assigned to four different groups. Thirty-two patients had defects on the femoral condyles, 16 on the trochlea, 11 on the tibia and 11 on the patella. Regarding the different parameters the four groups were relatively homogeneous: the average age ranged between 38.5 and 41.6 years, the body mass index between 25.2 and 26.4 kg/m2 and the defect size between 2.0 and 2.39 cm2. The details of the four study groups appear in Table I. INCLUSION CRITERIA
The criteria for inclusion were full-thickness chondral defects grade III A,B according to the International Cartilage Repair Society (ICRS)-classification system13 (International Cartilage Repair Society); that includes lesions extending down to the calcified layer (IIIB) but not through the subchondral bone plate (IIIC). The intact subchondral bone plate was detected preoperatively with an Magnetic resonance imaging (MRI), showing no subchondral edema or damage to the bone and intraoperatively with a probe by arthroscopic palpation. The lesions were sized between 1 and 4 cm2 and had to be localized in only one of the three knee compartments (medial femoro-tibial joint, lateral femoro-tibial joint or patello-femoral joint). Furthermore the study population was limited to patients between 18 and 55 years of age.
Each patient underwent the same standardized evaluation progress pre-, intra- and postoperatively using the modified Cincinnati-score (1 ¼ excellent, 2 ¼ good, 3 ¼ fair, 4 ¼ poor)14 and the ICRS-scoring system (1 ¼ normal, 2 ¼ nearly normal, 3 ¼ abnormal, 4 ¼ severely abnormal)13. For this purpose the patients had to answer standardized questionnaires and were examined by an orthopaedic surgeon preoperatively and 6, 18 and 36 months after surgery. The average follow-up was 36 months (range 34e38 months). Varus or valgus deformities were excluded by X-ray of the whole leg. The correct patella position was detected by a routine medio-lateral, patello-femoral and axial joints radiographs. Furthermore an MRI was performed preoperatively and 18 and 36 months after the surgical intervention. According to the classification system of Henderson et al. the following four criteria were evaluated: defect filling (1 ¼ complete, 2 50% of the defect, 3 < 50%, 4 ¼ full-thickness defect), cartilage signal (1 ¼ normal ¼ identical to the adjacent articular cartilage, 2 ¼ nearly normal ¼ slight areas of hyperintensity, 3 ¼ abnormal ¼ larger areas of hyperintensity, 4 ¼ absent), subchondral edema and effusion (both graded as 1 ¼ absent, 2 ¼ mild, 3 ¼ moderate, 4 ¼ severe)15. Additionally, an overall MRI-score was given, corresponding to the worst score in the four categories. The amount of fill reflects the growth of repair tissue, the signal might be an indicator of maturity of the graft e especially in comparison to the signal of the adjacent normal cartilage, the subchondral edema might reflect the attachment to the underlying bone, cartilage tears and the process of graft remodeling and the effusion is an indicator for chronic irritation or infection of the joint15. TREATMENT
EXCLUSION CRITERIA
Excluded were patients with a trauma within the last 4 weeks, varus or valgus deformities with a malalignment over 5(, limits in knee extension or flexion less than 130(, patella malalignment with medial or lateral shift of more than 0.5 cm, instabilities of the collateral or cruciate ligaments, meniscal pathologies, morphine treatment for more than 3 months, intra-articular corticosteroid injections
The microfracture was performed by two experienced surgeons as described by Steadman et al.1,2, who recommended to debride first the exposed bone of all remaining unstable cartilage using a curette and a full-radius resector to create a perpendicular edge of healthy well-attached viable cartilage around the defect. After preparation of the bed, the very small micro-holes were generated with an angular awl and distributed across the entire articular cartilage
Table I Preoperative patient information: the P-value between the different defect size, defect grade, body mass index and average age of the four groups was always >0.05 (ManneWhitney-U-test). This makes the four groups comparable Group 1 2 3 4
Localization of defect
Number of patients
Femoral condyles Trochlea Tibia Retropatellar
32 16 11 11
Average age (years) 38.7 41.6 39.7 38.5
(19e55) (26e55) (22e55) (23e55)
Male:female 17:15 8:8 3:8 5:6
Body mass index (kg/m2) 25.2 26.4 25.6 25.2
(19e31) (22e32) (21e29) (21e29)
Defect size (cm2) 2.02 2.31 2.39 2.0
(1e3) (1e4) (1.5e4) (1e3)
Outerbridge classification 3.75 3.94 3.64 3.73
(3e4) (3e4) (3e4) (3e4)
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Osteoarthritis and Cartilage Vol. 14, No. 11 lesion site, at a distance of 3e4 mm apart and down to a depth of 4 mm, thus yielding about 3e4 holes/cm2. Thus the biomechanics of the subchondral bone plate was not disturbed drastically. Finally the irrigation pump pressure was reduced to control efficient bleeding from all generated channels. One drain without suction was placed intra-articularly to reduce the risk of an arthrofibrosis in case of diffuse bleeding. The drain did not affect the postoperative passive range of motion since it was already removed on day 1 or 2 after microfracture depending on the amount of secretion. Postoperative mobilization was started on the first day after surgery with a continuous passive motion machine for 6e8 h/day16. For lesions on the weight-bearing surfaces on the condyles the initial range of motion was 30e60( and increased after 1 week as tolerated by 10e20( until full range of motion was obtained. For lesions of the patello-femoral joint the flexion was limited with a brace for 2 weeks to 40(, for another 2 weeks to 60( and until the sixth week after surgery to 90(. The brace prevents excessive shear forces on the maturing marrow clot. Cold therapy was used for all patients for 1 week. The patients were kept in hospital for 2e3 days after the surgical procedure. Low molecular weight heparin s.c. as well as non-steroidal anti-inflammatory medication were used. Crutch-assisted touchdown weight-bearing ambulation was prescribed for 6 weeks after the surgical procedure. Afterwards the patients progressed to full weight-bearing and began a more vigorous program of active motion of the knee. Crutch free walking was permitted after 3 months and return to sports was permitted after 4e6 months depending on the clinical examination. STATISTICAL ANALYSIS
Descriptive statistics during follow-up (arithmetic mean, standard deviation, range) were calculated using standard formulas. Baseline clinical scores were compared with follow-up data by paired Wilcoxon-tests and Friedman-tests for the modified Cincinnati knee score and the ICRS-score. The effects of patient age, body mass index, location, grade and size of lesion were assessed using Pearson correlation with post hoc independent samples ManneWhitney-U-test.
Table II ICRS- and Cincinnati-score preoperative and after 36 months in the four groups. Patients of group 1 improved significantly more ( P < 0.02) as patients in group 2, 3 or 4. Thirty-six months after microfracture the Pearson coefficient of correlation between both scores (overall) was 0.81 Group
Average ICRS-score preoperative
Average ICRS-score after 36 months
Average Cincinnatiscore preoperative
Average Cincinnatiscore after 36 months
1 2 3 4
3.53 0.51 3.88 0.34 3.91 0.3 3.64 0.5
2.13 0.75 3.06 1.0 3.0 0.77 2.91 0.83
4.0 0.0 4.0 0.0 4.0 0.0 4.0 0.0
1.66 0.87 2.94 1.29 2.55 1.04 2.55 0.93
Overall
3.69 0.47
2.6 0.92
4.0 0.0
2.23 113
Furthermore MRI-characteristics and clinical scores were compared using the Spearman coefficient of correlation17. All statistics were performed with SPSS and reviewed by an independent statistician.
Results All surgical procedures were performed without complications. Postoperatively, there were two patients with a temporary tingling around the arthroscopic portals, which disappeared completely after 3 months. Seven patients had a persisting effusion over 4 weeks that had to be treated with knee elevation, anti-inflammatory medication and cool dressings. There were no patients with postoperative infection or limited range of motion. There was a significant improvement in all groups between the preoperative scores and the scores at final follow-up (P < 0.0001). The Pearson coefficient of correlation between both scores (overall) was 0.81. However the Cincinnati-score improved more as the ICRS-score (P < 0.0001) (Table II). The Cincinnati-score increased in group 12.34 0.87 points, compared to 1.06 1.29 points in group 2 and 1.45 0.98 points in groups 3 and 4. Regarding the ICRS-score the patients of group 1 improved
Table III (a, b) Course of the ICRS- and Cincinnati-score between preoperative, 6, 18 and 36 months after microfracture. Listed is always the scoredelta D (with its P-value) between two intervals. Significant deterioration (in bold type) occured in both scores in all groups between 18 and 36 months postoperative except the patients of group 1. However regarding the whole study period of 36 months all groups improved significantly in both scores Group
Improvement between preoperative and 6 months postoperative ICRS-scoreD (P-value)
1 2 3 4
0.91 0.5 0.9 0.91
(<0.0001) (¼0.005) (¼0.002) (¼0.015)
Overall
079 (<0.0001)
Group
Cincinnati-scoreD (P-value) 1.94 1.5 1.82 1.73
(<0.0001) (<0.0001) (¼0.002) (¼0.002)
1.79 (<0.0001)
Improvement between 6 and 18 months postoperative ICRS-scoreD (P-value) 0.96 1.0 0.73 0.64
0.86 (<0.0001)
Deterioration between 18 and 36 months postoperative ICRS-scoreD (P-value)
1 2 3 4
0.47 0.68 0.73 0.82
Overall
0.56 (<0.0001)
(¼0.06) ([0.013) ([0.005) ([0.007)
Cincinnati-scoreD (P-value) 0.19 0.69 0.46 0.37
(¼0.217) ([0.022) ([0.013) ([0.046)
0.2 (¼0.059)
(<0.0001) (¼0.001) (¼0.005) (¼0.008)
Cincinnati-scoreD (P-value) 0.21 0.25 0.09 0.09
(¼0.008) (¼0.046) (¼0.317) (¼0.56)
0.18 (¼0.001)
Improvement between preoperative and 36 months postoperative ICRS-scoreD (P-value) 1.4 0.82 0.91 0.73
(<0.0001) (¼0.006) (¼0.008) (¼0.046)
1.09 (<0.0001)
Cincinnati-scoreD (P-value) 2.34 1.06 1.45 1.45
(<0.0001) (¼0.01) (¼0.008) (¼0.005)
1.77 (<0.0001)
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Fig. 1. Diagnostic arthroscopy 12 months after microfracture. The defect is filled with repair tissue, completely integrated and in level with the surrounding cartilage.
most as well. Patients of group 1 improved significantly more (P < 0.02) compared to patients of the other three groups (Table III) . With respect to the follow-up intervals the patients improved from preoperative to 6 months and from 6 to 18 months after microfracture (P < 0.05) (Fig. 1). However in groups 3 and 4 there was no more significant improvement in the Cincinnati-score in the second interval. In the third interval between 18 and 36 months after microfracture the course of both scores changed (Fig. 2). There was significant deterioration of the ICRS- and the Cincinnati-score in groups 2, 3 and 4 (P < 0.05). Only the patients of group 1 revealed neither a significant improvement nor a significant deterioration in both scores (P > 0.06) (Table III). However the older patients over 40 years of group 1 (n ¼ 16) deteriorated significantly in the ICRS-score (P ¼ 0.005). In this group younger patients (less than 40 years old; n ¼ 16) had a significantly better clinical outcome than did older patients (P ¼ 0.008) (Figs. 3 and 4). MRI 36 months after surgery revealed best defect filling in group 1 (Fig. 3) with significant difference when compared to the other groups (P < 0.02) (Table IV). The Pearson
Fig. 2. Diagnostic arthroscopy 3 years after microfracture. The repair tissue is soft and degenerated with large fissures and loose cartilage fibers.
Fig. 3. Sagittal T1-weighted MRI (repetition time, 567 ms; echo time, 15 ms) of the right knee of a 32-year-old woman 3 years after microfracture; the defect is completely filled and the signal of the repair tissue is identical to the adjacent articular cartilage. The former lesion is marked with two arrows.
coefficient of correlation between defect filling and ICRSscore was 0.84 and significant at the 0.01 level. The clinical scores 36 months after microfracture correlated best with the overall MRI-score and the MRI parameter ‘‘defect filling’’ (Table V).
Discussion Recent studies have revealed promising results after microfracture. In this context Steadman et al. described improved function in 95% of their study population with a mean follow-up of 11.3 years1. There was significant improvement in patients’ ability to do activities of daily living, strenuous work and sports from preoperative scores to scores obtained during follow-up after surgery. These results were astonishing since microfracture (as well as Pridie drilling and abrasion arthroplasty) belongs to the classical marrow stimulation techniques that involve surgical access to the bone marrow spaces underlying regions of damaged articular cartilage and thus promote resurfacing with
Fig. 4. Sagittal T1-weighted MRI (repetition time, 572 ms; echo time, 15 ms) of the right knee of a 48-year-old man 3 years after microfracture; on the medial femoral condyle is a full-thickness cartilage defect with no more repair tissue and a subchondral edema.
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Table IV MRI 36 months after surgery: the best defect filling could be detected in group 1 with significant difference when compared to the other groups ( P < 0.02). The Pearson coefficient of correlation between defect filling and subchondral edema was 0.89 and significant at the 0.01 level Group
Defect filling
Subchondral edema
Cartilage signal
Effusion
Overall MRI-score
1 2 3 4
1.69 0.74 2.56 0.96 2.64 0.92 2.55 0.93
1.50 0.62 2.31 0.96 2.55 0.93 2.45 1.04
1.63 0.61 2.31 0.94 2.55 0.93 2.36 0.92
1.31 0.47 1.88 0.62 2.36 1.03 2.18 0.98
1.78 0.71 2.56 0.96 2.64 0.92 2.64 1.03
Overall
2.17 0.95
2.0 0.93
2.04 0.88
1.74 0.81
2.23 0.94
predominantly fibrocartilaginous repair tissue of inferior quality. In this context a fibrous type of cartilage tissue has been found in rabbits3,10,18 and dogs19 that underwent abrasion chondroplasty20. The histological findings were identical in laboratory experiments with rabbits that underwent Pridie drilling21 or canines treated with microfracture22. There are only few studies that examine the durability of fibrous cartilage. In rabbits subjected to Pridie drilling, repair tissue endured for a longer period than did in animals treated by abrasion chondroplasty3. This may be due to the preserved subchondral bone plate between the drill holes with its biomechanical characteristics23. Shapiro examined the durability of fibrous tissue in 122 New Zealand white rabbits over a period of 48 weeks11. He found progressive differentiation of mesenchymal stem cells in fullthickness drilled defects of articular cartilage in fibroblasts, osteoblasts, articular chondroblasts and chondrocytes within the first 12 weeks. However between 24 and 48 weeks after surgical intervention progressive failure of apparently well healed cartilage occurred. Reason for the worse durability was the lack of physical and chemical bonding between the macromolecular components of the repair tissue and the residual adjacent cartilage allowing micromotion and macromotion between them. Furthermore he found that the repair cartilage over the re-established prominent tidemark was only half as thick as the surrounding original cartilage. Since bone is more than 1000 times stiffer than cartilage the thin and soft repair tissue is predisposed to degenerate over the hard and hypertrophic subchondral bone plate11,24,25 (Fig. 5). These results could be confirmed by a recent sheep study with microfracture of created cartilage lesions. The initially well formed repair tissue degenerated over a stiff and hypertrophic subchondral bone plate after a period of 12 months12. Similar results could be detected in a recent prospective cohort study with microfracture of 48 isolated cartilage defects of the femur: MRI evaluation revealed osseous overgrowth in 25% of the patients and persistent gaps between the native and repair tissue in 92% of the microfracture repairs26. In the control MRI’s of our study population we detected an osseous overgrowth in 19 of all 70 patients. These results confirm and may explain the outcome of our study: good results with high score levels after 6 and 18 months deteriorated after the study period of 36 months.
However also the population of Steadman’s study included patients without improvement: 17% considered the pain in their knees unchanged as compared with the preoperative status and 4% considered the pain worse postoperatively; 53.5% of all patients reported about mild and 14.1% about moderate pain. Swelling decreased from preoperative scores up to year 3 but did not change from years 3 through 7. Seven percent of all knees had to undergo a second surgery for persistent swelling and discomfort1. This heterogenity in outcome between worse and excellent results over more than 10 years could be explained by some factors influencing the final result: until now the structure of the tissue formed after microfracture is still unclear. Recent histological studies in an equine model have shown the microfracture repair cartilage to be not only fibrous but a mixture of fibrocartilage (48%) and hyaline cartilage (20%)27. Knutsen found in a randomized trial comparing microfracture and ACI more fibrous as hyaline cartilage in the histological evaluation of biopsy specimens taken during a second-look arthroscopy after microfracture. Fifty percent of the biopsies in the ACI group showed some hyaline tissue. For the small number of biopsies and the short-term follow-up of 2 years there was no significant difference in the histological results between both groups9. Peterson found in his ACI-study 80% hyaline cartilage in the biopsies, analysed by independent pathologists28,29. In the study of Brittberg et al., 11 of 15 patients had ‘‘hyaline-like cartilage’’ after ACI30. Frisbie et al. found 70% type II collagen at 1 year after microfracture, however the aggrecan content was less than ideal27. The described differences in the structure of the repair tissue may lead to different results because of changing biomechanical qualities: the stiffness of hyaline cartilage is 3.07 N , of hyaline-like cartilage 2.77 N and of fibrous cartilage 1.27 N31. Glaser and Putz have shown that the reduced stiffness of
Table V Pearson coefficient of correlation between MRI-characteristics and the clinical scores 36 months after microfracture. The defect filling and the overall MRI-score correlated best with the clinical symptoms. All correlations were significant at the 0.01 level Score
ICRS Cincinnati
Defect filling 0.84 0.87
Subchondral Cartilage Effusion edema signal 0.76 0.77
0.76 0.75
0.71 0.69
Overall MRIscore 0.85 0.85
Fig. 5. Intralesional osteophytes as result of osseous growth into the defect site after microfracture with thinning the overlying repair tissue.
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fibrocartilage leads to fissures in the tissue texture and thus to progressive osteoarthritis32. Besides the quality of the repair tissue some other factors may influence the result. An age over 35 years1, atrophic muscles with insufficient knee stabilization and missing continuous passive motion16,18,20,33 turned out to be disadvantageous. Compared to Steadman’s patients our study population was less sportive and the mean age was higher. Furthermore our patients underwent serial objective observation instead of a subjective evaluation by questionnaires. Finally the ICRS-score is more critical as the Cincinnatiscore since the lowest grade within a group determines the group grade. These factors may explain the deterioration of results in our study group compared to Steadman’s study group. For the disappointing results after microfracturing patellofemoral chondral lesions, we tend to perform alternative treatment methods in this compartment. In chondral lesions over 2 cm2 we use for the patella different techniques of ACI and for the trochlea ACI as well or autologous osteochondral transplantation33e36. However all resurfacing techniques may have success only if the biomechanical properties of the joint with tibiofemoral or patella malalignment and ligament instabilities are considered and treated as well33,34. The worse results of patients over 40 years compared to younger patients may be explained by the reduced regeneration capacity of the repair tissue. As stem cells age, their telomere length, mitochondrial function and their mitotic and synthetic activity decline, and their responsiveness to anabolic mechanical stimuli and growth factors decreases37,38. For these reasons chondrocyte senescence contributes to the age-related increase in the prevalence of osteoarthritis and decrease in the efficacy of cartilage repair. Therefore we have limited the indication for the microfracture procedure in older patients to chondral lesions smaller than 2 cm2. In larger lesions microfracture might have only the potential to relieve pain for some years or to delay the implantation of an endoprosthesis. Microfracture is a minimal invasive and cheap method with good short-term results especially in young active patients with small cartilage defects. A deterioration of the results starts 18 months after surgery and is most evident in the ICRS-score. The best prognostic factors have young patients with defects on the femoral condyles.
Acknowledgments No support in form of grants, equipment or other items has occurred for this project. The authors have received nothing of value. This manuscript does not contain information about medical devices.
References 1. Steadman JR, Briggs KK, Rodrigo JJ, Kocher MS, Gill TJ, Rodkey WG. Outcomes of microfracture for traumatic chondral defects of the knee: average 11-year follow-up. Arthroscopy 2003;19:477e84. 2. Steadman JR, Miller BS, Karas SG, Schlegel TF, Briggs KK, Hawkins RJ. The microfracture technique in the treatment of full-thickness chondral lesions of the knee in National Football League players. J Knee Surg 2003;16:83e6.
3. Menche D, Frenkel S, Blair B, Watnik N, Toolan B, Yahhoubian R, et al. A comparison of abrasion arthroplasty and subchondral drilling in the treatment of fullthickness cartilage lesions in the rabbit. Arthroscopy 1996;12:280e6. 4. Pridie KH. A method of resurfacing osteoarthritic knee joints. J Bone Joint Surg Br 1959;41:618e9. 5. Tippet JW. Articular cartilage drilling and osteotomy in osteoarthritis of the knee. In: McGinty JB, Caspari RB, Jackson RW, Poehling GG, Eds. Operative Arthroscopy. 2nd edn. Philadelphia, New York: Raven Press 1996:411e26. 6. Sledge SL. Microfracture techniques in the treatment of osteochondral injuries. Clin Sports Med 2001;20: 365e77. 7. Hunziker EB. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 2002;10: 432e63. 8. Knutsen G, Engebretsen L, Ludvigsen TC, Drogset JO, Grontvedt T, Solheim E, et al. Autologous chondrocyte implantation versus microfracture e a prospective randomised Norwegian multicenter-trial. ICRSSymposium June 2002, Toronto, Canada Orthopaedics Today Intern 2002;5:25. 9. Knutsen G, Engebretsen L, Ludvigsen TC, Drogset JO, Grontvedt T, Solheim E, et al. Autologous chondrocyte implantation compared with microfracture in the knee. A randomized trial. J Bone Joint Surg Am 2004;86(3): 455e64. 10. Furukawa T, Eyre DR, Koide S, Glimcher MJ. Biochemical studies on repair cartilage resurfacing experimental defects in the rabbit knee. J Bone Joint Surg 1980; 62A:79e89. 11. 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;75A: 532e53. 12. Nehrer S, Dorotka R, Bindreiter U, Losert U, Windberger U, Macfelda K, et al. Microfracture in the treatment of chondral defects in a sheep model. Abstract book of the 5th symposium of the International Cartilage Repair Society in Gent, Belgium, 2004; p. 42. 13. Brittberg M, Aglietti P, Gambardella R, Hangody L, Hauselmann HJ, Jakob RP, et al. The ICRS clinical cartilage injury evaluation system e 2000. 3rd ICRS meeting in Go¨teborg, Sweden, 2000. 14. Noyes FR, McGinniss GH, Grood ES. The variable functional disability of the anterior cruciate ligamentdeficient knee. Orthop Clin North Am 1985;16:47e67. 15. Henderson IJP, Tuy B, Connell D, Oakes B, Hettwer WH. Prospective clinical study of autologous chondrocyte implantation and correlation with MRI at three and 12 months. J Bone Joint Surg Br 2003; 85B:1060e6. 16. Rodrigo JJ, Steadman JR, Silliman JF, Fulstone HA. Improvement in full-thickness chondral defect healing in the human knee after debridement and microfracture using continuous passive motion. Am J Knee Surg 1994;7:109e16. 17. Hosmer DW, Lemeshow S. Applied Logistic Regression. New York: John Wiley 1989. pp. 106e43. 18. Kim HWK, Moran ME, Salter RB. The potential for regeneration of articular cartilage in defects created by chondral shaving and subchondral abrasion e an experimental investigation in rabbits. J Bone Joint Surg 1991;73A:1301e15.
Osteoarthritis and Cartilage Vol. 14, No. 11 19. Altman R, Kates J, Chun L, Dean D, Eyre D. Preliminary observations of chondral abrasion in a canine model. Ann Rheum Dis 1992;51:1056e62. 20. Johnson L. Arthroscopic abrasion arthroplasty historical and pathologic perspective: present status. Arthroscopy 1986;2:54e69. 21. Hice G, Freedman D, Lemont H, Khoury S. Scanning and light microscopic study of irrigated and nonirrigated joints following burr surgery performed through a small incision. J Foot Surg 1990;29:337e44. 22. Breinan H, Martin S, Spector M. Healing of canine articular cartilage defects treated with microfracture, a type-II collagen matrix, or cultured autologous chondrocytes. J Orthop Res 2000;18:781e9. 23. Rand JA. Role of arthroscopy in osteoarthritis of the knee. Arthroscopy 1991;7:358e63. 24. Wong M, Hunziker EB. Articular cartilage biology and biomechanics. In: Erggelet C, Steinwachs M, Eds. Gelenkknorpeldefekte. Darmstadt: Steinkopf Press 2001:15e27. 25. Simon W. Scale effects in animal joints. I. Articular cartilage thickness and compressive stress. Arthritis Rheum 1970;13:244e56. 26. Mithoefer K, Williams RJ III, Warren RF, Potter HG, Spock CR, Jones EC, et al. The microfracture technique for the treatment of articular cartilage lesions in the knee. J Bone Joint Surg Am 2005;87A(9): 1911e20. 27. Frisbie DD, Trotter GW, Powers BE. Arthroscopic subchondral bone plate microfracture technique augments healing of large chondral defects in the radial carpal bone and medial femoral condyle of horses. Vet Surg 1999;28:242e55. 28. Peterson L. Autologous chondrocyte transplantation e long term results. In: Hendrich C, No¨th U, Eulert J, Eds. Cartilage Surgery and Future Perspectives. Heidelberg, New York: Springer Press 2003:19e27. 29. Peterson L, Minas T, Brittberg M, Nilsson A, Sjo¨grenJansson E, Lindahl A. Two-to-9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop 2000;374:212e34.
1125 30. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994;331:889e95. 31. Peterson L, Brittberg M, Kiviranta I, Lundgren Akerlund E, Lindahl A. Autologous chondrocyte transplantation. Biomechanics and long-term durability. Am J Sports Med 2002;30:2e12. 32. Glaser C, Putz R. Functional anatomy of articular cartilage under compressive loading. Quantitative aspects of global, local and zonal reactions of the collagenous network with respect to the surface integrity. Osteoarthritis Cartilage 2002;10:83e99. 33. Steinwachs MR, Kreuz PC. Combinations of different cartilage resurfacing techniques. Z Orthop Ihre Grenzbeg 2003;141:625e8. 34. Steinwachs MR, Kreuz PC. Clinical results of ACT using a collagen membrane. In: Hendrich C, No¨th U, Eulert C, Eds. Cartilage Surgery and Future Perspectives. Berlin, Heidelberg, New York: Springer Press 2003:37e47. 35. Kreuz PC, Steinwachs M, Erggelet C, Lahm A, Henle P, Niemeyer P. Mosaicplasty with autogenous talar autograft for osteochondral lesions of the talus after failed primary arthroscopic management. A prospective study with a 4-years follow-up. Am J Sports Med 2005;33(12):1e9. 36. Kreuz PC, Steinwachs MR, Edlich M, Kaiser T, Mika J, Lahm A, et al. The anterior approach for the treatment of posterior osteochondral lesions of the talus: comparison of different surgical techniques. Arch Orthop Trauma Surg 2006;126:241e6. 37. Maneiro E, Martin MA, de Andres MC, LopezArmada MJ, Fernandez-Sueiro JL, del Hoyo P, et al. Mitochondrial respiratory activity is altered in osteoarthritic human articular chondrocytes. Arthritis Rheum 2003;48(3):700e8. 38. Martin JA, Buckwalter JA. The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. J Bone Joint Surg Am 2003; 85-A(Suppl 2):106e10.
International Cartilage Repair Society
Results after microfracture of full-thickness chondral defects in different compartments in the knee P. C. Kreuz M.D.y*, M. R. Steinwachs Ph.D.y, C. Erggelet Ph.D.y, S. J. Krausey, G. Konrad M.D.y, M. Uhl M.D.z and N. Su¨dkamp Ph.D.y y Department of Orthopaedic and Trauma Surgery, Albert Ludwig University Freiburg, Hugstetterstrasse 55, 79106 Freiburg, Germany z Department of Radiology, Albert Ludwig University Freiburg, Hugstetterstrasse 55, 79106 Freiburg, Germany Summary Objective: To determine if the clinical results after microfracture of full-thickness cartilage lesions deteriorate over a period of 36 months. Methods: Between 1999 and 2002 85 patients (mean age 39.5 years) with full-thickness cartilage lesions underwent the microfracture procedure and were evaluated preoperatively and 6, 18 and 36 months after surgery. Exclusion criteria were meniscal pathologies, axial malpositioning and ligament instabilities. Baseline clinical scores were compared with follow-up data by paired Wilcoxon-tests for the modified Cincinnati knee and the International Cartilage Repair Society (ICRS)-score. The effects of the lesion localization and Magnetic resonance imaging (MRI) parameters were evaluated using the Pearson correlation and independent samples tests. Results: Both scores revealed significant improvement 18 months after microfracture (P < 0.0001). Within the second 18 months after surgery there was a significant deterioration in the ICRS-score (P < 0.0001). The best results could be observed in chondral lesions of the femoral condyles. Defects in other areas of the knee deteriorated between 18 and 36 months after microfracture. MRI 36 months after surgery revealed best defect filling in lesions on the femoral condyles with significant difference in the other areas (P < 0.02). The Pearson coefficient of correlation between defect filling and ICRS-score was 0.84 and significant at the 0.01 level. Conclusions: Microfracture is a minimal invasive method with good short-term results in the treatment of small cartilage defects. A deterioration of the results starts 18 months after surgery and is most evident in the ICRS-score. The best prognostic factors have young patients with defects on the femoral condyles. ª 2006 Published by Elsevier Ltd on behalf of OsteoArthritis Research Society International. Key words: Osteoarthritis, Marrow stimulation technique, Microfracture, Cartilage lesion.
but partially preserved between the microfracture holes improving load-bearing characteristics following healing3. In contrast to Pridie drilling no heat necrosis or polishing is introduced into the subchondral bone and marrow with microfracture4,5. The equipment is standardized and the costs are minimal since expensive cell cultures are not necessary. Unlike osteochondral, perichondral, periosteal or chondral autograft procedures the problem of a harvest site morbidity is excluded6. The intervention leads to a spontaneous repair response, which is based upon therapeutically induced bleeding from the opened subchondral bone spaces and subsequent blood-clot formation7. Knutsen has compared in a recent study the histological results after microfracture and autologous chondrocyte implantation (ACI). The predominant repair tissue after microfracture was fibrocartilage. For the small number of biopsies and the short-term follow-up of 2 years there was no significant difference in the histological results after ACI8,9. Furthermore animal studies have shown that the tissue formed after microfracture is fibrous in nature10 and not durable11,12. Therefore a long-term cure cannot be expected from the performance of this marrow stimulation technique. Regardless of these poor biomechanical prerequisites recent studies with long-term follow-up over 10 years
Introduction Microfracture is one of many methods available to treat articular cartilage lesions. The technique has been elaborated by Steadman et al. and applied chiefly in young athletes and in young patients generally1,2. There are some inherent advantages. The microfracture technique is minimally invasive because it is arthroscopic through standard portals in most cases. In comparison to an abrasion chondroplasty the subchondral bone plate is not completely destructed 1
Parts of the study were presented at the nineteenth and twentyfirst annual congress of the International Society for Orthopaedics Traumatology and Sports Medicine, Munich, Germany, June 2004 and May 2006 at the first common annual congress for orthopaedic and trauma surgery, Berlin, Germany, October 2005, and at the sixth ICRS-symposium (International Cartilage Repair Society) in San Diego, USA, January 2006. No support in form of grants, equipment or other items has occurred for this project. *Address correspondence and reprint requests to: Peter Cornelius Kreuz, M.D., Department of Orthopaedic Surgery, Albert Ludwig University of Freiburg, Hugstetterstrasse 55, 79106 Freiburg, Germany. Tel: 49-761-270-2401; Fax: 49-761-270-2619; E-mail: [email protected] Received 21 June 2005; revision accepted 9 May 2006.
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have shown improvement in function without significant deterioration over the time. However these studies are only functional outcome case series of patients with chondral lesions, based on special self-administered questionnaires sent to the patients after surgical intervention4. There is only one prospective study with a 2-year followup and a serial objective observation by clinical and histological evaluation9. The present prospective study is based on scores with a continuous objective patient evaluation including control MRI’s over a period of 36 months.
Patients and methods
within the previous month or knee arthroscopy within the previous 6 months. STUDY DESIGN
The prospective study with a 36-months follow-up was conducted to determine the efficacy of microfracture in the postoperative follow-up. Furthermore we wished to figure out if primary good results 6 or 12 months after surgery remain on the same level or deteriorate after a period of 36 months. STUDY COURSE
Between 1999 and 2002 a total of 85 patients with fullthickness chondral defects of the knee underwent the microfracture procedure. Thereof 70 patients (33 males, 37 females) with an average age of 39.5 years (range 19e55 years) met the inclusion criteria (below). Depending on the localization of the defects (femoral condyles, trochlea, tibia or retropatellar) the patients were assigned to four different groups. Thirty-two patients had defects on the femoral condyles, 16 on the trochlea, 11 on the tibia and 11 on the patella. Regarding the different parameters the four groups were relatively homogeneous: the average age ranged between 38.5 and 41.6 years, the body mass index between 25.2 and 26.4 kg/m2 and the defect size between 2.0 and 2.39 cm2. The details of the four study groups appear in Table I. INCLUSION CRITERIA
The criteria for inclusion were full-thickness chondral defects grade III A,B according to the International Cartilage Repair Society (ICRS)-classification system13 (International Cartilage Repair Society); that includes lesions extending down to the calcified layer (IIIB) but not through the subchondral bone plate (IIIC). The intact subchondral bone plate was detected preoperatively with an Magnetic resonance imaging (MRI), showing no subchondral edema or damage to the bone and intraoperatively with a probe by arthroscopic palpation. The lesions were sized between 1 and 4 cm2 and had to be localized in only one of the three knee compartments (medial femoro-tibial joint, lateral femoro-tibial joint or patello-femoral joint). Furthermore the study population was limited to patients between 18 and 55 years of age.
Each patient underwent the same standardized evaluation progress pre-, intra- and postoperatively using the modified Cincinnati-score (1 ¼ excellent, 2 ¼ good, 3 ¼ fair, 4 ¼ poor)14 and the ICRS-scoring system (1 ¼ normal, 2 ¼ nearly normal, 3 ¼ abnormal, 4 ¼ severely abnormal)13. For this purpose the patients had to answer standardized questionnaires and were examined by an orthopaedic surgeon preoperatively and 6, 18 and 36 months after surgery. The average follow-up was 36 months (range 34e38 months). Varus or valgus deformities were excluded by X-ray of the whole leg. The correct patella position was detected by a routine medio-lateral, patello-femoral and axial joints radiographs. Furthermore an MRI was performed preoperatively and 18 and 36 months after the surgical intervention. According to the classification system of Henderson et al. the following four criteria were evaluated: defect filling (1 ¼ complete, 2 50% of the defect, 3 < 50%, 4 ¼ full-thickness defect), cartilage signal (1 ¼ normal ¼ identical to the adjacent articular cartilage, 2 ¼ nearly normal ¼ slight areas of hyperintensity, 3 ¼ abnormal ¼ larger areas of hyperintensity, 4 ¼ absent), subchondral edema and effusion (both graded as 1 ¼ absent, 2 ¼ mild, 3 ¼ moderate, 4 ¼ severe)15. Additionally, an overall MRI-score was given, corresponding to the worst score in the four categories. The amount of fill reflects the growth of repair tissue, the signal might be an indicator of maturity of the graft e especially in comparison to the signal of the adjacent normal cartilage, the subchondral edema might reflect the attachment to the underlying bone, cartilage tears and the process of graft remodeling and the effusion is an indicator for chronic irritation or infection of the joint15. TREATMENT
EXCLUSION CRITERIA
Excluded were patients with a trauma within the last 4 weeks, varus or valgus deformities with a malalignment over 5(, limits in knee extension or flexion less than 130(, patella malalignment with medial or lateral shift of more than 0.5 cm, instabilities of the collateral or cruciate ligaments, meniscal pathologies, morphine treatment for more than 3 months, intra-articular corticosteroid injections
The microfracture was performed by two experienced surgeons as described by Steadman et al.1,2, who recommended to debride first the exposed bone of all remaining unstable cartilage using a curette and a full-radius resector to create a perpendicular edge of healthy well-attached viable cartilage around the defect. After preparation of the bed, the very small micro-holes were generated with an angular awl and distributed across the entire articular cartilage
Table I Preoperative patient information: the P-value between the different defect size, defect grade, body mass index and average age of the four groups was always >0.05 (ManneWhitney-U-test). This makes the four groups comparable Group 1 2 3 4
Localization of defect
Number of patients
Femoral condyles Trochlea Tibia Retropatellar
32 16 11 11
Average age (years) 38.7 41.6 39.7 38.5
(19e55) (26e55) (22e55) (23e55)
Male:female 17:15 8:8 3:8 5:6
Body mass index (kg/m2) 25.2 26.4 25.6 25.2
(19e31) (22e32) (21e29) (21e29)
Defect size (cm2) 2.02 2.31 2.39 2.0
(1e3) (1e4) (1.5e4) (1e3)
Outerbridge classification 3.75 3.94 3.64 3.73
(3e4) (3e4) (3e4) (3e4)
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Osteoarthritis and Cartilage Vol. 14, No. 11 lesion site, at a distance of 3e4 mm apart and down to a depth of 4 mm, thus yielding about 3e4 holes/cm2. Thus the biomechanics of the subchondral bone plate was not disturbed drastically. Finally the irrigation pump pressure was reduced to control efficient bleeding from all generated channels. One drain without suction was placed intra-articularly to reduce the risk of an arthrofibrosis in case of diffuse bleeding. The drain did not affect the postoperative passive range of motion since it was already removed on day 1 or 2 after microfracture depending on the amount of secretion. Postoperative mobilization was started on the first day after surgery with a continuous passive motion machine for 6e8 h/day16. For lesions on the weight-bearing surfaces on the condyles the initial range of motion was 30e60( and increased after 1 week as tolerated by 10e20( until full range of motion was obtained. For lesions of the patello-femoral joint the flexion was limited with a brace for 2 weeks to 40(, for another 2 weeks to 60( and until the sixth week after surgery to 90(. The brace prevents excessive shear forces on the maturing marrow clot. Cold therapy was used for all patients for 1 week. The patients were kept in hospital for 2e3 days after the surgical procedure. Low molecular weight heparin s.c. as well as non-steroidal anti-inflammatory medication were used. Crutch-assisted touchdown weight-bearing ambulation was prescribed for 6 weeks after the surgical procedure. Afterwards the patients progressed to full weight-bearing and began a more vigorous program of active motion of the knee. Crutch free walking was permitted after 3 months and return to sports was permitted after 4e6 months depending on the clinical examination. STATISTICAL ANALYSIS
Descriptive statistics during follow-up (arithmetic mean, standard deviation, range) were calculated using standard formulas. Baseline clinical scores were compared with follow-up data by paired Wilcoxon-tests and Friedman-tests for the modified Cincinnati knee score and the ICRS-score. The effects of patient age, body mass index, location, grade and size of lesion were assessed using Pearson correlation with post hoc independent samples ManneWhitney-U-test.
Table II ICRS- and Cincinnati-score preoperative and after 36 months in the four groups. Patients of group 1 improved significantly more ( P < 0.02) as patients in group 2, 3 or 4. Thirty-six months after microfracture the Pearson coefficient of correlation between both scores (overall) was 0.81 Group
Average ICRS-score preoperative
Average ICRS-score after 36 months
Average Cincinnatiscore preoperative
Average Cincinnatiscore after 36 months
1 2 3 4
3.53 0.51 3.88 0.34 3.91 0.3 3.64 0.5
2.13 0.75 3.06 1.0 3.0 0.77 2.91 0.83
4.0 0.0 4.0 0.0 4.0 0.0 4.0 0.0
1.66 0.87 2.94 1.29 2.55 1.04 2.55 0.93
Overall
3.69 0.47
2.6 0.92
4.0 0.0
2.23 113
Furthermore MRI-characteristics and clinical scores were compared using the Spearman coefficient of correlation17. All statistics were performed with SPSS and reviewed by an independent statistician.
Results All surgical procedures were performed without complications. Postoperatively, there were two patients with a temporary tingling around the arthroscopic portals, which disappeared completely after 3 months. Seven patients had a persisting effusion over 4 weeks that had to be treated with knee elevation, anti-inflammatory medication and cool dressings. There were no patients with postoperative infection or limited range of motion. There was a significant improvement in all groups between the preoperative scores and the scores at final follow-up (P < 0.0001). The Pearson coefficient of correlation between both scores (overall) was 0.81. However the Cincinnati-score improved more as the ICRS-score (P < 0.0001) (Table II). The Cincinnati-score increased in group 12.34 0.87 points, compared to 1.06 1.29 points in group 2 and 1.45 0.98 points in groups 3 and 4. Regarding the ICRS-score the patients of group 1 improved
Table III (a, b) Course of the ICRS- and Cincinnati-score between preoperative, 6, 18 and 36 months after microfracture. Listed is always the scoredelta D (with its P-value) between two intervals. Significant deterioration (in bold type) occured in both scores in all groups between 18 and 36 months postoperative except the patients of group 1. However regarding the whole study period of 36 months all groups improved significantly in both scores Group
Improvement between preoperative and 6 months postoperative ICRS-scoreD (P-value)
1 2 3 4
0.91 0.5 0.9 0.91
(<0.0001) (¼0.005) (¼0.002) (¼0.015)
Overall
079 (<0.0001)
Group
Cincinnati-scoreD (P-value) 1.94 1.5 1.82 1.73
(<0.0001) (<0.0001) (¼0.002) (¼0.002)
1.79 (<0.0001)
Improvement between 6 and 18 months postoperative ICRS-scoreD (P-value) 0.96 1.0 0.73 0.64
0.86 (<0.0001)
Deterioration between 18 and 36 months postoperative ICRS-scoreD (P-value)
1 2 3 4
0.47 0.68 0.73 0.82
Overall
0.56 (<0.0001)
(¼0.06) ([0.013) ([0.005) ([0.007)
Cincinnati-scoreD (P-value) 0.19 0.69 0.46 0.37
(¼0.217) ([0.022) ([0.013) ([0.046)
0.2 (¼0.059)
(<0.0001) (¼0.001) (¼0.005) (¼0.008)
Cincinnati-scoreD (P-value) 0.21 0.25 0.09 0.09
(¼0.008) (¼0.046) (¼0.317) (¼0.56)
0.18 (¼0.001)
Improvement between preoperative and 36 months postoperative ICRS-scoreD (P-value) 1.4 0.82 0.91 0.73
(<0.0001) (¼0.006) (¼0.008) (¼0.046)
1.09 (<0.0001)
Cincinnati-scoreD (P-value) 2.34 1.06 1.45 1.45
(<0.0001) (¼0.01) (¼0.008) (¼0.005)
1.77 (<0.0001)
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Fig. 1. Diagnostic arthroscopy 12 months after microfracture. The defect is filled with repair tissue, completely integrated and in level with the surrounding cartilage.
most as well. Patients of group 1 improved significantly more (P < 0.02) compared to patients of the other three groups (Table III) . With respect to the follow-up intervals the patients improved from preoperative to 6 months and from 6 to 18 months after microfracture (P < 0.05) (Fig. 1). However in groups 3 and 4 there was no more significant improvement in the Cincinnati-score in the second interval. In the third interval between 18 and 36 months after microfracture the course of both scores changed (Fig. 2). There was significant deterioration of the ICRS- and the Cincinnati-score in groups 2, 3 and 4 (P < 0.05). Only the patients of group 1 revealed neither a significant improvement nor a significant deterioration in both scores (P > 0.06) (Table III). However the older patients over 40 years of group 1 (n ¼ 16) deteriorated significantly in the ICRS-score (P ¼ 0.005). In this group younger patients (less than 40 years old; n ¼ 16) had a significantly better clinical outcome than did older patients (P ¼ 0.008) (Figs. 3 and 4). MRI 36 months after surgery revealed best defect filling in group 1 (Fig. 3) with significant difference when compared to the other groups (P < 0.02) (Table IV). The Pearson
Fig. 2. Diagnostic arthroscopy 3 years after microfracture. The repair tissue is soft and degenerated with large fissures and loose cartilage fibers.
Fig. 3. Sagittal T1-weighted MRI (repetition time, 567 ms; echo time, 15 ms) of the right knee of a 32-year-old woman 3 years after microfracture; the defect is completely filled and the signal of the repair tissue is identical to the adjacent articular cartilage. The former lesion is marked with two arrows.
coefficient of correlation between defect filling and ICRSscore was 0.84 and significant at the 0.01 level. The clinical scores 36 months after microfracture correlated best with the overall MRI-score and the MRI parameter ‘‘defect filling’’ (Table V).
Discussion Recent studies have revealed promising results after microfracture. In this context Steadman et al. described improved function in 95% of their study population with a mean follow-up of 11.3 years1. There was significant improvement in patients’ ability to do activities of daily living, strenuous work and sports from preoperative scores to scores obtained during follow-up after surgery. These results were astonishing since microfracture (as well as Pridie drilling and abrasion arthroplasty) belongs to the classical marrow stimulation techniques that involve surgical access to the bone marrow spaces underlying regions of damaged articular cartilage and thus promote resurfacing with
Fig. 4. Sagittal T1-weighted MRI (repetition time, 572 ms; echo time, 15 ms) of the right knee of a 48-year-old man 3 years after microfracture; on the medial femoral condyle is a full-thickness cartilage defect with no more repair tissue and a subchondral edema.
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Table IV MRI 36 months after surgery: the best defect filling could be detected in group 1 with significant difference when compared to the other groups ( P < 0.02). The Pearson coefficient of correlation between defect filling and subchondral edema was 0.89 and significant at the 0.01 level Group
Defect filling
Subchondral edema
Cartilage signal
Effusion
Overall MRI-score
1 2 3 4
1.69 0.74 2.56 0.96 2.64 0.92 2.55 0.93
1.50 0.62 2.31 0.96 2.55 0.93 2.45 1.04
1.63 0.61 2.31 0.94 2.55 0.93 2.36 0.92
1.31 0.47 1.88 0.62 2.36 1.03 2.18 0.98
1.78 0.71 2.56 0.96 2.64 0.92 2.64 1.03
Overall
2.17 0.95
2.0 0.93
2.04 0.88
1.74 0.81
2.23 0.94
predominantly fibrocartilaginous repair tissue of inferior quality. In this context a fibrous type of cartilage tissue has been found in rabbits3,10,18 and dogs19 that underwent abrasion chondroplasty20. The histological findings were identical in laboratory experiments with rabbits that underwent Pridie drilling21 or canines treated with microfracture22. There are only few studies that examine the durability of fibrous cartilage. In rabbits subjected to Pridie drilling, repair tissue endured for a longer period than did in animals treated by abrasion chondroplasty3. This may be due to the preserved subchondral bone plate between the drill holes with its biomechanical characteristics23. Shapiro examined the durability of fibrous tissue in 122 New Zealand white rabbits over a period of 48 weeks11. He found progressive differentiation of mesenchymal stem cells in fullthickness drilled defects of articular cartilage in fibroblasts, osteoblasts, articular chondroblasts and chondrocytes within the first 12 weeks. However between 24 and 48 weeks after surgical intervention progressive failure of apparently well healed cartilage occurred. Reason for the worse durability was the lack of physical and chemical bonding between the macromolecular components of the repair tissue and the residual adjacent cartilage allowing micromotion and macromotion between them. Furthermore he found that the repair cartilage over the re-established prominent tidemark was only half as thick as the surrounding original cartilage. Since bone is more than 1000 times stiffer than cartilage the thin and soft repair tissue is predisposed to degenerate over the hard and hypertrophic subchondral bone plate11,24,25 (Fig. 5). These results could be confirmed by a recent sheep study with microfracture of created cartilage lesions. The initially well formed repair tissue degenerated over a stiff and hypertrophic subchondral bone plate after a period of 12 months12. Similar results could be detected in a recent prospective cohort study with microfracture of 48 isolated cartilage defects of the femur: MRI evaluation revealed osseous overgrowth in 25% of the patients and persistent gaps between the native and repair tissue in 92% of the microfracture repairs26. In the control MRI’s of our study population we detected an osseous overgrowth in 19 of all 70 patients. These results confirm and may explain the outcome of our study: good results with high score levels after 6 and 18 months deteriorated after the study period of 36 months.
However also the population of Steadman’s study included patients without improvement: 17% considered the pain in their knees unchanged as compared with the preoperative status and 4% considered the pain worse postoperatively; 53.5% of all patients reported about mild and 14.1% about moderate pain. Swelling decreased from preoperative scores up to year 3 but did not change from years 3 through 7. Seven percent of all knees had to undergo a second surgery for persistent swelling and discomfort1. This heterogenity in outcome between worse and excellent results over more than 10 years could be explained by some factors influencing the final result: until now the structure of the tissue formed after microfracture is still unclear. Recent histological studies in an equine model have shown the microfracture repair cartilage to be not only fibrous but a mixture of fibrocartilage (48%) and hyaline cartilage (20%)27. Knutsen found in a randomized trial comparing microfracture and ACI more fibrous as hyaline cartilage in the histological evaluation of biopsy specimens taken during a second-look arthroscopy after microfracture. Fifty percent of the biopsies in the ACI group showed some hyaline tissue. For the small number of biopsies and the short-term follow-up of 2 years there was no significant difference in the histological results between both groups9. Peterson found in his ACI-study 80% hyaline cartilage in the biopsies, analysed by independent pathologists28,29. In the study of Brittberg et al., 11 of 15 patients had ‘‘hyaline-like cartilage’’ after ACI30. Frisbie et al. found 70% type II collagen at 1 year after microfracture, however the aggrecan content was less than ideal27. The described differences in the structure of the repair tissue may lead to different results because of changing biomechanical qualities: the stiffness of hyaline cartilage is 3.07 N , of hyaline-like cartilage 2.77 N and of fibrous cartilage 1.27 N31. Glaser and Putz have shown that the reduced stiffness of
Table V Pearson coefficient of correlation between MRI-characteristics and the clinical scores 36 months after microfracture. The defect filling and the overall MRI-score correlated best with the clinical symptoms. All correlations were significant at the 0.01 level Score
ICRS Cincinnati
Defect filling 0.84 0.87
Subchondral Cartilage Effusion edema signal 0.76 0.77
0.76 0.75
0.71 0.69
Overall MRIscore 0.85 0.85
Fig. 5. Intralesional osteophytes as result of osseous growth into the defect site after microfracture with thinning the overlying repair tissue.
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P. C. Kreuz et al.: Microfracture in full-thickness chondral defects
fibrocartilage leads to fissures in the tissue texture and thus to progressive osteoarthritis32. Besides the quality of the repair tissue some other factors may influence the result. An age over 35 years1, atrophic muscles with insufficient knee stabilization and missing continuous passive motion16,18,20,33 turned out to be disadvantageous. Compared to Steadman’s patients our study population was less sportive and the mean age was higher. Furthermore our patients underwent serial objective observation instead of a subjective evaluation by questionnaires. Finally the ICRS-score is more critical as the Cincinnatiscore since the lowest grade within a group determines the group grade. These factors may explain the deterioration of results in our study group compared to Steadman’s study group. For the disappointing results after microfracturing patellofemoral chondral lesions, we tend to perform alternative treatment methods in this compartment. In chondral lesions over 2 cm2 we use for the patella different techniques of ACI and for the trochlea ACI as well or autologous osteochondral transplantation33e36. However all resurfacing techniques may have success only if the biomechanical properties of the joint with tibiofemoral or patella malalignment and ligament instabilities are considered and treated as well33,34. The worse results of patients over 40 years compared to younger patients may be explained by the reduced regeneration capacity of the repair tissue. As stem cells age, their telomere length, mitochondrial function and their mitotic and synthetic activity decline, and their responsiveness to anabolic mechanical stimuli and growth factors decreases37,38. For these reasons chondrocyte senescence contributes to the age-related increase in the prevalence of osteoarthritis and decrease in the efficacy of cartilage repair. Therefore we have limited the indication for the microfracture procedure in older patients to chondral lesions smaller than 2 cm2. In larger lesions microfracture might have only the potential to relieve pain for some years or to delay the implantation of an endoprosthesis. Microfracture is a minimal invasive and cheap method with good short-term results especially in young active patients with small cartilage defects. A deterioration of the results starts 18 months after surgery and is most evident in the ICRS-score. The best prognostic factors have young patients with defects on the femoral condyles.
Acknowledgments No support in form of grants, equipment or other items has occurred for this project. The authors have received nothing of value. This manuscript does not contain information about medical devices.
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