Background Full-thickness defects of articular cartilage inthe knee have a poor capacity for repair. They may progressto osteoarthritis and require total knee replacement. We performedautologous chondrocyte transplantation in 23 people with deepcartilage defects in the knee.
Methods The patients ranged in age from 14 to 48 years and hadfull-thickness cartilage defects that ranged in size from 1.6to 6.5 cm2. Healthy chondrocytes obtained from an uninvolvedarea of the injured knee during arthroscopy were isolated andcultured in the laboratory for 14 to 21 days. The cultured chondrocyteswere then injected into the area of the defect. The defect wascovered with a sutured periosteal flap taken from the proximalmedial tibia. Evaluation included clinical examination accordingto explicit criteria and arthroscopic examination with a biopsyof the transplantation site.
Results Patients were followed for 16 to 66 months (mean, 39).Initially, the transplants eliminated knee locking and reducedpain and swelling in all patients. After three months, arthroscopyshowed that the transplants were level with the surroundingtissue and spongy when probed, with visible borders. A secondarthroscopic examination showed that in many instances the transplantshad the same macroscopic appearance as they had earlier butwere firmer when probed and similar in appearance to the surroundingcartilage. Two years after transplantation, 14 of the 16 patientswith femoral condylar transplants had good-to-excellent results.Two patients required a second operation because of severe centralwear in the transplants, with locking and pain. A mean of 36months after transplantation, the results were excellent orgood in two of the seven patients with patellar transplants,fair in three, and poor in two; two patients required a secondoperation because of severe chondromalacia. Biopsies showedthat 11 of the 15 femoral transplants and 1 of the 7 patellartransplants had the appearance of hyaline cartilage.
Conclusions Cultured autologous chondrocytes can be used torepair deep cartilage defects in the femorotibial articularsurface of the knee joint.
Full-thickness defects of articular cartilage in the knee mayprogress to osteoarthritis. In 1743 Hunter1 stated, "From Hippocratesto the present age it is universally allowed that ulceratedcartilage is a troublesome thing and that, once destroyed, isnot repaired." Articular cartilage defects are still a practicalproblem, especially in younger patients, and correlate withpain and joint dysfunction2.
Injuries of the knee cartilage leading to osteoarthritis includelesions disrupting both cartilage and subchondral bone (osteochondrallesions) and lesions limited to the cartilage tissue (chondrallesions). Chondral and osteochondral lesions are both commonafter trauma3,4,5,6. Repeated minor trauma, as well as overtinjury of the knee, can cause osteoarthritis7,8,9.
When osteoarthritis is severe, the usual treatment is replacementof the arthritic articular surface with an artificial prosthesis.Total knee replacement is most commonly performed in peopleover 60 years of age. Treatment of younger patients (under theage of 50 years) is more troublesome, because the prostheseshave a limited lifetime10,11. Transplanted heterologous or autologouschondrocytes,12,13,14 periosteum, perichondrium,15,16 and osteochondralgrafts are potential treatments for focal articular cartilagedefects. These approaches have been studied in animals. A 1984study in rabbits reported successful treatment of focal patellardefects with the use of transplanted cultured autologous chondrocytes17.The cultured chondrocytes were injected under a periosteal flapsutured over the defect. One year after transplantation, newlyformed cartilage-like tissue typically covered about 70 percentof the defect18,19. Encouraged by these results, we used chondrocytetransplantation to treat 23 patients with deep cartilage defectsin their knees.
Methods
The transplantation procedure is outlined in Figure 1. The studywas approved by the ethics committee of the Medical Faculty,University of Goteborg. In accordance with Swedish law, patientswere informed of the nature of the study and gave their oralconsent. All patients had cartilage defects down to, but notthrough, the subchondral bone, on a load-bearing surface ofthe femoral condyle or the patellar facet (Figure 2A), withdisabling symptoms of the knee, including locking, localizedpain, swelling, and retropatellar crepitus.
Figure 2. Results of Autologous Chondrocyte Transplantation in a 22-Year-Old Woman (Patient 9).
Panel A shows the cartilage defect in the medial femoral condyle before cell transplantation. Panel B shows the defect (1.1 by 4.0 cm) 46 months after transplantation. The borders of the transplant are indicated by the arrows. Knee surgery was performed at 46 months because of patellar trauma that was unrelated to the transplantation.
Twenty-three patients (11 men and 12 women) with a mean ageof 27 years (range, 14 to 48) were treated for a mean periodof 44 months (range, 12 to 120) after the initial arthroscopicdetection of the injury (Figure 3A). Thirteen patients had defectsof the femoral condyle primarily due to trauma, and three hadlocalized osteochondral lesions due to abnormalities of theunderlying bone (osteochondritis dissecans). The other sevenpatients had painful defects of the patellar facet: six hadchondromalacia patellae (grade IV, according to the Outerbridgeclassification20), and one had a defect of traumatic origin.The defects ranged in size from 1.6 to 6.5 cm2 (mean, 3.1).Ten of the patients had previously undergone shaving and debridementof fibrillated cartilage and unstable chondral flaps, with atransient improvement in symptoms.
Figure 3. Arthroscopic View of a Femoral Condylar Defect before Transplantation (Panel A) and 22 Months after Transplantation (Panel B) in a 40-Year-Old Man (Patient 7).
Isolation and Culture of Chondrocytes
With the patients under general anesthesia, surgery was performedin a tourniquet-controlled, bloodless field. Cartilage slices(weight, 300 to 500 mg) were obtained through an arthroscopefrom a minor load-bearing area on the upper medial femoral condyleof the damaged knee.
The cartilage was placed in chilled sterile 0.9 percent (weightper volume) sodium chloride. Cells were isolated within twoto five hours. Cartilage specimens were minced and washed threetimes in culture medium containing Ham's F12 medium supplementedwith HEPES buffer (10 mmol per liter), gentamicin sulfate (50µg per milliliter [approximately 70 µmol per liter]),amphotericin B (2 µg per milliliter [2.2 µmol perliter]), and l-ascorbic acid (50 µg per milliliter [300µmol per liter]). The minced cartilage was digested for16 hours in a spinner bottle in 10 ml of culture medium containingclostridial collagenase (1 mg per milliliter [150 U per liter])and deoxyribonuclease I (0.1 mg per milliliter [25,000 U perliter]). The cells were then filtered through nylon mesh witha pore diameter of 25 microm, washed three times, counted (range,180,000 to 455,000 cells), resuspended in culture medium supplementedwith 15 percent of the patient's serum (autologous serum), andseeded at a cell density of 5000 to 10,000 cells per squarecentimeter in 25-cm2 or 75-cm2 culture flasks (Costar, Cambridge,Mass.).
The culture medium was changed twice weekly and tested for bacterialgrowth on blood-agar plates after one week. During the 24 hoursbefore culturing, antibiotics were omitted from the culturemedium so that bacterial contamination, if present, would bemore likely to be detected.
Transplantation took place 14 to 21 days after the initial surgery.Chondrocytes were suspended by means of treatment with trypsin,pelleted in a centrifuge, and washed three times in culturemedium supplemented with 20 percent autologous serum. Afterthe last centrifugation, the cell suspension was aspirated intoa 1-ml tuberculin syringe (Terumo, Leuven, Belgium) with a 1.2-mmneedle. The final volume of the cell suspension was 50 to 100microl, with a total of 2.6 million to 5 million cells. Thechondrogenic phenotype (determined by microscopical evaluationof clonal growth and metachromatic staining) was studied ina minor fraction of the isolated cells, which were placed ina suspension culture stabilized with agarose for three weeks.
Transplantation of Chondrocytes
Prophylactic antibiotics were given intravenously in three dosesover a 24-hour period during and after the surgery. Most ofthe patients received cloxacillin (1 g given three times). Patientswho were allergic to penicillin received clindamycin (600 mggiven three times) instead. With the patients under generalanesthesia, a medial or lateral parapatellar arthrotomy wasperformed in a tourniquet-controlled, bloodless field. The chondrallesion was excised as far as the normal surrounding cartilagebut not as far as the subchondral bone plate. The cartilagedefect was covered with a periosteal flap taken from the proximalmedial tibia. The flap was sutured to the surrounding rim ofthe normal cartilage with interrupted 5-0 Dexon sutures. Thecultured chondrocytes were injected beneath the periosteal flap.The joint capsule, retinaculum layer, and skin were suturedin separate layers. The knee was covered with a small elasticbandage. Active movement of the knee without weight bearingwas initiated two to three days after surgery. Weight bearingwas gradually introduced and increased to the full extent, withisometric quadriceps training, during the first eight weeksafter surgery.
Evaluation
Patients were evaluated every 8 to 12 weeks, and the conditionof the knee was graded as excellent (no pain, swelling, or lockingwith strenuous activity), good (mild aching with strenuous activitybut no swelling or locking), fair (moderate pain with strenuousactivity and occasional swelling but no locking), or poor (painat rest, swelling, and locking).
Postoperative arthroscopy was performed 3 months after the surgeryand was repeated 12 to 46 months after the surgery. The hardnessof the transplant was tested with the tip of a probing hook,and the extent of repair of the tissue was documented macroscopicallyon videotape. The gross appearance was considered biologicallyacceptable if the cartilage defect was filled with cartilaginoustissue that was in contact with, as well as level with, thesurrounding articular cartilage21.
During the second arthroscopic procedure, biopsy specimens extendingto the subchondral bone were taken from the central part ofthe transplant. The specimens were fixed in 5 percent formaldehyde,embedded in paraffin, sectioned, and stained with Weigert'siron hematoxylin, van Gieson's solution, and Alcian blue. Thearticular cartilage appeared red with this staining. Histologicsections were coded and examined by a pathologist who was unawareof the study.
Immunohistochemical staining for type II collagen was performedin biopsy specimens from five patients (Patients 11, 13, 14,15, and 16) (Table 1). Normal articular cartilage was used asa positive control, and periosteum as a negative control. Thefirst antibody was omitted to control for nonspecific bindingof the second antibody. Three monoclonal antibodies were tested(CIIB1, CIIC1, and CIIC2; courtesy of Professor L. Klareskog,University of Uppsala, Uppsala, Sweden). These antibodies recognizethree different epitopes on native type II collagen22 (datanot shown).
Table 1. Femoral Condylar Defects in 16 Patients Treated with Transplanted Chondrocytes.
Results
The results of chondrocyte transplantation in the 16 patientswith femoral defects are summarized in Table 1, and the resultsof transplantation in the 7 patients with patellar transplantsare summarized in Table 2. The cells placed in agarose culturesdemonstrated clonal growth with metachromatic staining of thesurrounding matrix (data not shown). None of the cell culturescontained bacteria or fungi, and none of the patients had kneeinfections after the transplantation.
Table 2. Patellar Defects in Seven Patients Treated with Transplanted Chondrocytes.
The patients were followed for 16 to 66 months (mean, 39). Inall the patients, knee pain, swelling, and crepitation wereconsiderably reduced, and knee locking completely disappeared.The initial arthroscopy, performed three months after the transplantation,showed regenerated areas of cartilage with visible borders thatwere level with the surrounding articular surface. The colorand texture of the transplanted area were similar to those ofthe surrounding, undamaged cartilage. In the central area ofthe transplant, a soft indentation, without subchondral bonecontact, was felt with probing. In most cases, there were wavelikemovements of the transplant area when it was probed, suggestingthat the transplant was loosely attached to the underlying bone.In Patient 1, the condylar transplant, which had loosened, wassutured to the surrounding articular cartilage six months afterthe initial surgery. Ten months later, one third of the transplantwas removed, because it was still loose and causing lockingof the knee.
Femoral Condylar Transplants
Two years after transplantation, 14 of the 16 patients had resultsthat were graded either excellent (in 6 patients) or good (in8). The two patients followed for the longest period had excellentresults 55 and 59 months after transplantation. The second arthroscopy,performed 12 to 46 months (mean, 24) after transplantation,showed that in the 14 patients with excellent or good results,the transplants had a biologically acceptable gross appearancewith visible borders and were level with the surrounding articularcartilage (Figure 3B). The transplants and the surrounding cartilagefelt similarly firm when probed, and wavelike movements of thetransplants were no longer observed.
In Patients 1 and 3 (Table 1) severe central wear developedin the transplants, with locking of the knee and pain, 14 and11 months, respectively, after transplantation. Both patientsrequired a second operation. Degenerative tissue was debridedand resurfaced with subchondral drill holes filled with carbon-fiberimplants23. Six months after this additional surgery, the resultsin both patients were graded fair. The knee joint in Patient9 (Table 1) was opened 46 months after transplantation becauseof a patellar injury, unrelated to the treated defect, whichcaused recurrent instability. The transplant was slightly whiterthan the surrounding articular cartilage and when probed hada resistance to pressure similar to that of the surroundingcartilage (Figure 2B). This patient underwent surgical realignmentof the patella, and six months later the results were gradedexcellent.
Biopsy specimens were obtained from 15 of the 16 patients withfemoral transplants. The specimens from 11 of the patients hadan intact articular surface and a hyaline appearance, with chondrocytesin lacunae and metachromatic staining comparable with that ofthe surrounding cartilage (Figure 4). These findings indicatethat the transplanted cells and the periosteum were able toregenerate normal hyaline cartilage in the area of the defect.In most of the biopsy specimens, remnants of the periostealtissue were seen close to the articular surface. Specimens fromfour patients contained areas of irregular fibrous tissue surroundedby more hyaline-like tissue. The results of immunohistochemicaltesting for type II collagen in biopsy specimens from five patientswere positive, and the results in the control specimens werenegative (data not shown).
Figure 4. Histologic Section from a Biopsy Specimen Obtained 36 Months after Surgery in a 19-Year-Old Man with a Femoral Condylar Defect (Patient 16).
The articular surface is at the top of the section, with newly formed cartilage in the lower part of the section and a thin layer of remaining periosteal tissue in between. The cartilage defect was approximately 4 mm deep before transplantation (Weigert's iron hematoxylin, van Gieson, and Alcian blue). The scale bar represents 100 microm.
Patellar Transplants
The results of transplantation in the seven patients with patellardefects were graded excellent or good in two, fair in three,and poor in two at a mean follow-up of 36 months (range, 24to 66) after transplantation. Five patients had improved kneefunction after the transplantation, largely because they hadno locking. The second arthroscopic procedure (performed a meanof 19 months after surgery) revealed an acceptable gross appearanceof the transplants in three of these five patients and centralwear in two. The two patients with poor transplantation results(Patients 18 and 21) (Table 2) had severe chondromalacia andrequired a second operation with debridement and surgical resectionof the failed graft and subchondral bone combined with the implantationof carbon-fiber pads23 16 and 24 months, respectively, aftertransplantation. The results in these two patients were fairsix months after surgery.
Only one of the seven patients with patellar transplants hada biopsy specimen with an intact articular surface and a hyalineappearance with metachromatic staining comparable with thatof the surrounding cartilage. The biopsy specimens from theother six patients had central areas of irregular fibrous tissuesurrounded by more hyaline-like tissue.
Discussion
More than 500,000 arthroplastic procedures and total joint replacementsare performed each year in the United States, including about95,000 total knee replacements and 41,000 other procedures torepair defects of the knee24. If the treatment of cartilageinjuries of the knee at an early stage could prevent the developmentof osteochondritis, the need for a total joint replacement mightbe postponed or eliminated.
We performed autologous chondrocyte transplantation in 23 patientswith isolated defects of knee cartilage due to trauma or osteochondritisdissecans. After three years of follow-up, the transplants restoredconsiderable knee function in 14 of the 16 patients with femoraldefects. The treatment resulted in the formation of new cartilagethat was similar to normal cartilage in that it had an abundanceof type II collagen and metachromatically stained matrix. Thedetection of immunoreactivity to type II collagen in biopsyspecimens from the regenerated tissue is an important finding;type II collagen fibers, unlike type I fibers, are criticalfor the macromolecular framework of the extracellular matrixthat gives articular (i.e., hyaline) cartilage its unique biomechanicalproperties.
The results in the seven patients with patellar transplantswere disappointing. Five patients had improved joint function,but only two had a good or excellent outcome.
To minimize the potential side effects of the treatment, weused autologous chondrocytes cultured in autologous serum. Studiesof transplantation in animals with the use of allogeneic chondrocyteshave had conflicting results; immunologic rejection of the transplantis possible25,26,27,28. The use of autologous chondrocytes alsominimized the likelihood of transmitting infectious diseases.
The chondrogenic cells in the transplant may be able to repaircartilage more efficiently than the chondrocytes at the marginof the injured cartilage. The culturing procedure increasedthe number of chondrocytes initially isolated by 10 to 20 times.A fraction of the cultured cells were able to reexpress theirchondrogenic phenotype, after the use of culturing proceduresknown to facilitate the production of cartilage matrix. Theseresults are similar to those obtained with the use of rabbitarticular chondrocytes in a similar culture protocol29.
Articular resurfacing techniques that have been used to helprepair cartilage include subchondral drilling, abrasion, andthe procedure termed "spongialization" (excision of diseasedpatellar cartilage and subchondral bone, leaving well-vascularizedcancellous bone exposed)30,31,32. The tissue that results fromthese reparative techniques is disorganized fibrocartilaginoustissue with type I collagen fibers33,34 that is unable to restorethe biomechanical properties of normal articular cartilage35.
The use of periosteal or perichondrial grafts as a treatmentfor localized cartilage defects in animals has resulted in theformation of chondroid tissue with metachromatic staining ofthe extracellular matrix36,37. However, the results of transplantationwith both periosteum and perichondrium are inconsistent16,38,39.
In our study the treatment of chondromalacia patellae (in whichthe defect of the cartilage is confined to the patella) wasless successful than the treatment of femoral condylar defectscaused by trauma. One possible explanation is that the patellardefects we treated had different causes -- that is, malalignmentof the patellae with a lateral hyperpressure syndrome, patellarlateral subluxation, osteochondral injury, osteoarthritis,40or greater contact stress in the patellofemoral joint than inthe tibiofemoral articulation. The correction of underlyingjoint abnormalities concomitantly with the transplantation ofchondrocytes may improve the success rate for patients withpatellar defects. Similar considerations apply to cartilageinjuries with ligament instability in the femorotibial compartment.
The mechanism of the repair process is unknown. The biopsiesindicate that new cartilage is formed close to the underlyingcalcified cartilage and bone and is clearly distinguishablefrom remnants of the periosteum. There are at least three theoreticalexplanations for the repair process. One explanation is thatthe transplanted cells consist of chondrocytes that are ableto repopulate the area of the defect and produce new cartilagematrix; the function of the periosteum is only to seal off thedefect. A second explanation is that the periosteum stimulatesthe replication of the transplanted cultured chondrocytes. Athird explanation is that the periosteum and transplanted cellsstimulate chondrocytes in the surrounding cartilage or cellsin the deep noncalcified and calcified layers of the articularcartilage or in the periosteum itself to enter the area of thedefect, divide, and repair the defect. The importance of thetransplanted cells to the repair process is supported by previousstudies in rabbits, which showed that periosteum alone couldnot repair defective cartilage17,18,19.
Our results indicate that cultured autologous chondrocytes canbe used to repair articular cartilage defects in the femorotibialjoint and that this treatment restores the function of the jointby forming predominantly hyaline-like cartilage containing typeII collagen.
Supported by grants from the Lundberg Foundation, Swedish MedicalResearch Council, Trygg Hansa Research Foundation, King GustafV Eightieth Birthday Fund, and Assar Gabrielsson Research Foundation.
We are indebted to Drs. Howard Green, Ben Bronstein, and JimRheinwald for their critical comments and helpful suggestions.
Source Information
From the Departments of Orthopedic Surgery (M.B., A.N., L.P.), Clinical Chemistry (A.L.), and Internal Medicine (C.O., O.I.), Research Center for Endocrinology and Metabolism, University of Goteborg, Sahlgrenska University Hospital, Goteborg, Sweden. Presented at the first meeting of the Osteoarthritis Research Society, Paris, Dec.10-12, 1992.
Address reprint requests to Dr. Lindahl at the Research Center for Endocrinology and Metabolism, Department of Clinical Chemistry, Sahlgrenska University Hospital, S-413 45 Goteborg, Sweden.
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