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Intermediate Results of Large Cystic Medial Osteochondral Lesions of the Talus Treated With Osteoperiosteal Cylinder Autografts From the Medial Tibia
Original Article With Video Illustration
Intermediate Results of Large Cystic Medial Osteochondral Lesions of the Talus Treated With Osteoperiosteal Cylinder Autografts From the Medial Tibia Wan Chen, Ph.D., Kanglai Tang, M.D., Ph.D., Chengsong Yuan, M.D., You Zhou, Ph.D., and Xu Tao, M.D.
Purpose: To investigate the clinical and radiologic outcomes of an autologous osteoperiosteal cylinder graft from the medial tibia for the treatment of large cystic medial osteochondral lesions (OCLs) of the talus. Methods: The study included 15 patients with large cystic medial OCLs. All underwent medial malleolus osteotomy and excision and curettage of the defect site, followed by transplantation with an autologous osteoperiosteal cylinder graft from the medial tibia. They were evaluated preoperatively and after a minimum of 24 months (mean, 44.8 months; range, 24 to 72 months) postoperatively by a visual analog scale, the American Orthopaedic Foot & Ankle Society ankle-hindfoot scale, the OgilvieHarris scale, and magnetic resonance imaging of the ankle. Results: The mean visual analog scale score decreased from 5.40 1.06 points to 1.00 1.00 points (P < .001), and the mean American Orthopaedic Foot & Ankle Society score increased from 49.00 8.96 points to 89.00 4.17 points (P < .001). The mean Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART) score was 64.00 5.07 points. According to the Ogilvie-Harris scale, 7 cases were rated as excellent, 5 as good, 3 as fair, and 0 as poor. No complications were observed. Conclusions: An autologous osteoperiosteal cylinder graft from the medial tibia is effective for treating large cystic medial OCLs of the talus and has a low rate of complications. Level of Evidence: Level IV, case series.
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arge cystic osteochondral lesions (OCLs) of the talus pose a treatment challenge because drilling or debridement alone cannot treat the structural bony defect or restore subchondral support. Graft implantation offers the advantage of restoring the bony integrity. Current options for graft treatment of large cystic medial OCLs of the talus include osteochondral allograft transplantation,1 autologous osteochondral transplantation,2 chondrocyte transplantation, and other grafts from the autologous iliac crest3 and medial calcaneus.4 However, all of these options have disadvantages, such as a high rate of graft incorporation
From the Department of Orthopaedic Surgery, Southwest Hospital, Third Military Medical University, Chongqing, China. The authors report that they have no conflicts of interest in the authorship and publication of this article. Received July 10, 2014; accepted February 19, 2015. Address correspondence to Kanglai Tang, M.D., Ph.D., Department of Orthopaedic Surgery, Southwest Hospital, Third Military Medical University, Chongqing 400038, China. E-mail: [email protected] Ó 2015 by the Arthroscopy Association of North America 0749-8063/14582/$36.00 http://dx.doi.org/10.1016/j.arthro.2015.02.027
failure,1,5 high cost, donor-site morbidity,6 necessity for a 2-stage procedure, and the technically demanding process of graft preparation.1 Recently, we developed a novel technique involving an autologous osteoperiosteal cylinder graft from the medial tibia to repair a large cystic medial OCL of the talus. By comparing postoperative symptom relief, functional improvement, cartilage repair (based on magnetic resonance imaging [MRI]), and complications, this study aimed to investigate the clinical and radiologic outcomes of autologous osteoperiosteal cylinder grafts from the medial tibia used to treat large cystic medial OCLs of the talus. We hypothesized that this novel technique for treating large cystic medial OCLs of the talus using autologous osteoperiosteal cylinder grafts from the medial tibia would result in reduced pain levels, improved function, and improved appearance on MRI.
Methods Patients and Study Design A prospective clinical study was designed. The inclusion criteria for patients consisted of the following: a
Arthroscopy: The Journal of Arthroscopic and Related Surgery, Vol
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Table 1. Patient Details Defect Size Case No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Age, yr 34 55 34 27 32 33 25 46 52 51 49 43 37 34 51
Sex F M M M M M M F M M M F F M M
Side R R R L L R R L R R L R R R R
Diameter, mm, Depth, mm 14.01 14.62 13.43 18.54 11.24 18.26 15.67 19.37 14.44 18.85 15.61 17.99 16.03 18.69 14.77 16.07 14.84 17.87 14.52 18.29 15.44 18.64 12.38 14.67 13.45 15.44 15.87 13.56 15.32 14.39
Volume, mm3 2,252.648 2,625.013 1,810.936 3,733.682 3,085.428 3,441.174 3,770.04 2,751.988 3,089.314 3,027.029 3,488.271 1,764.985 2,192.611 2,680.916 2,651.234
Follow-up Time, mo 36 36 72 60 48 60 48 48 36 36 60 36 48 24 24
NOTE. Volume ¼ p (Diameter/2)2 Depth. F, Female; L, left; M, male; R, right.
type V OCL according to the Scranton and McDermott classification system; an OCL located in the medial talus; and failure to respond to nonoperative treatment (rest, immobilization, anti-inflammatory medication, or physical therapy) for at least 6 months. The exclusion criteria consisted of the following: age younger than 14 years or older than 60 years; presence of osteoporosis; presence of osteoarthritis, rheumatoid arthritis, arthrolithiasis, or related conditions; and presence of a lower limb malalignment. Between October 2008 and February 2012, 15 patients (11 men and 4 women; age range, 25 to 55 years; mean age, 40.2 years; 4 left and 11 right ankles) with large cystic medial OCLs of the talus were included in this prospective clinical and radiologic study. The demographic data, defect size, and follow-up time of each patient were recorded (Table 1). All patients reported ankle pain, and 5 patients reported a history of ankle sprain. The preoperative radiographs showed no other injury, and MRI showed large cystic medial OCLs of the talus. The operation and clinical follow-up were conducted by 2 senior surgeons (K.T., X.T.). The diameter of each cyst was measured on coronal, sagittal, and axial MRI scans, and the largest diameter measured for each cyst was considered. The depth of each cyst was measured on coronal and sagittal MRI scans, and the largest depth measured for each cyst was considered (Fig 1). The study was approved by the Clinical Academic Committee of the Third Military Medical University Southwest Hospital. Surgical Techniques After induction with combined spinal and epidural anesthesia, each patient was placed in the supine position with a tourniquet on the affected thigh (Video 1, available at www.arthroscopyjournal.org). A 10-cm curved longitudinal incision was made over the
medial malleolus. The medial malleolus was exposed by retracting the skin and separating the subcutaneous tissue. Two Kirschner wires were predrilled from the tip of the medial malleolus to the proximal tibia for medial malleolus fixation after osteotomy (Fig 2A). After extraction of the Kirschner wires, the osteotomy orientation of the lateral plane and anteroposterior plane was determined by fluoroscopy. An oblique osteotomy was performed with a microsagittal saw. The osteotomized medial malleolus was then reflected plantarward on the deltoid ligament to expose the medial aspect of the talar dome. The talar dome was inspected to identify the soft point (the cystic lesion surface) by probing. One Kirschner wire was drilled into the middle of the soft point, and a cannulated drill was used to create a small bone socket. The diameter and depth of the recipient socket were determined by MRI before the operation. In addition, all necrotic sequestra and tissue were curetted until bloody marrow oozed from the bone (Fig 2B). The donor site was determined at a location approximately 1.5 cm above the osteotomy plane. At a location approximately 1.5 cm above the osteotomy plus the diameter of the defect, one Kirschner wire was vertically drilled into the tibia. Before use of a trephine with a diameter 1 mm larger than the one used to drill a socket in the talar dome, the periosteum around the trephine apex was incised to avoid damaging the periosteum. The length of the osteoperiosteal cylinder graft harvested from the tibia by the trephine was 1 mm longer than the depth of the socket in the talar dome (Fig 2C). When the graft diameter was larger than 1.5 cm, an allograft was necessary to backfill the donor site.
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LARGE CYSTIC MEDIAL OSTEOCHONDRAL LESIONS
Fig 1. Magnetic resonance imaging scans of cystic osteochondral lesion of talus. The osteochondral lesion is located in the medial talus, and the subchondral cyst is surrounded by bone edema. The cyst measurements are as follows: (A) diameter of 12.02 mm and depth of 15.65 mm on the sagittal image, (B) diameter of 8.89 mm and depth of 16.07 mm on the coronal image, and (C) diameter of 14.77 mm on the axial image. The magnetic resonance imaging scans were measured using a picture archiving and communication system, and the diameter and depth are 14.77 mm and 16.07 mm, respectively. (A, anterior; FL, left foot; FA, anterior view of the foot.)
The graft was inserted into the bone socket of the talus (Fig 2D), and the graft stability was confirmed. Two Kirschner wires were placed into the hole of the medial malleolus, and the osteotomized medial malleolus was reduced. Two cannulated screws (General Care, Shanghai, China) were driven from the tip of the medial malleolus into the cancellous bone of the tibia. The anatomic reduction was confirmed by fluoroscopy. The wounds were closed in a routine manner, and sterile compression dressings were applied. Rehabilitation The postoperative regimen included noneweightbearing activity for 12 weeks. Weight-bearing activity was allowed after clinical and radiologic confirmation of solid union of the osteotomy. Screw extraction was performed after a minimum of 1 year. Clinical Evaluation We used a standard 10-point visual analog scale (VAS) and the American Orthopaedic Foot & Ankle Society (AOFAS) ankle-hindfoot scale to evaluate the symptoms and functional level of each patient before and a minimum of 24 months after surgery. All patients received an MRI scan before and a minimum of 24 months after surgery. The MRI parameters were as follows: repetition time, 600 milliseconds; echo time, 26 milliseconds; field of view, 180 160 mm; thickness, 3 mm; matrix, 192 128; and scanner tesla rating, 0.2 T. In addition, 2 musculoskeletal radiologists independently used the Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART) scoring system to evaluate the degree of defect repair and the integrity of
the subchondral bone at a minimum of 24 months after surgery. There were no significant differences between the 2 radiologists’ results. The mean score was used as the final score. The results of the operation were evaluated using the Ogilvie-Harris scale score for pain, swelling, stiffness, limping, and activity and were categorized as excellent, good, fair, or poor. For each patient, the lowest value among the individual categories was used as the final score. Statistical analysis was performed using SPSS software, version 13.0 (IBM, Armonk, NY). Paired-samples t tests and the Mann-Whitney U test were used to compare the VAS scores and AOFAS scores, respectively, before and after the procedures. The level of significance was set at 95%; P < .05 was considered significant.
Results According to the previously described criteria, 27 patients with noncystic OCLs, 6 with lateral OCLs, 8 with lateral noncystic OCLs, 17 with large medial cystic OCLs with osteoarthritis, and 2 with large medial cystic OCLs with lower limb malalignment were excluded, whereas 15 patients were included and treated with autologous osteoperiosteal cylinder grafts from the medial tibia. The mean time of follow-up was 44.8 months (range, 24 to 72 months). No patients were lost to follow-up. The mean VAS score improved from 5.40 1.06 points preoperatively to 1.00 1.00 points 2 years postoperatively (P < .001). The mean AOFAS score improved from 49.00 8.96 points preoperatively to 89.00 4.17 points 2 years postoperatively
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Fig 2. Graft harvest technique in a left foot. (A) Two Kirschner wires were predrilled for medial malleolus fixation after osteotomy. (B) A cannulated drill was used to create a small bone socket. (C) A trephine with a diameter larger than the one used to create a socket in the talar dome was used to drill into the tibia and harvest the osteoperiosteal cylinder graft. (D) The graft was inserted into the bone socket of the talus.
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LARGE CYSTIC MEDIAL OSTEOCHONDRAL LESIONS Table 2. Clinical Evaluation of Patients VAS Score Case No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean Total
AOFAS Score
Preoperative
Postoperative
Preoperative
Postoperative
MOCART Score
Ogilvie-Harris Scale Score
7 6 5 5 7 4 6 5 5 4 7 4 6 5 5 5.40 1.06 81
3 2 0 0 0 1 1 0 2 0 2 0 2 1 1 1.00 1.00 15
40 42 47 46 40 59 41 45 65 58 40 57 40 60 55 49.00 8.96 735
80 83 93 90 90 90 86 95 85 91 87 95 90 90 90 89.00 4.17 1,335
55 55 70 65 65 65 60 70 60 70 60 70 65 65 65 64.00 5.07 1,024
Fair Fair Excellent Excellent Good Excellent Good Excellent Fair Excellent Good Excellent Good Good Excellent
NOTE. For each patient, the lowest item of the Ogilvie-Harris score determines the final score. AOFAS, American Orthopaedic Foot & Ankle Society; MOCART, Magnetic Resonance Observation of Cartilage Repair Tissue; VAS, visual analog scale.
(P < .001) (Table 2, Fig 3). The mean Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART) score was 64.00 5.07 points. On the basis of the Ogilvie-Harris scale, 7 cases were rated as excellent, 5 as good, 3 as fair, and 0 as poor (Table 2). After 2 years, all MRI scans showed complete filling of the defects and complete integration with the adjacent native cartilage, as well as an intact surface and structure of the repaired tissue (Fig 4). No complications were observed.
Discussion Our results showed that autologous osteoperiosteal cylinder grafts from the medial tibia were an effective treatment for large cystic medial OCLs of the talus, resulting in pain relief, functional improvement, and
Fig 3. After the operation, the visual analog scale (VAS) score significantly decreased (P < .001) in 11 patients and the American Orthopaedic Foot & Ankle Society (AOFAS) score significantly increased (P < .001) in all 15 patients.
incorporation of the grafts and complete filling of the defects. Osteochondral defects with small subchondral cysts can be treated effectively with arthroscopic microfracture or abrasion arthroplasty, so definition of “large cystic” is a cutoff for an OCL size that is not fit for microfracture or other conservative treatment. Many studies have shown that the defect size is a significant predictor of outcome.7-13 In a study of lesions smaller than 15 mm by Chuckpaiwong et al.,10 excellent results were obtained in response to microfracture for OCLs of the ankle. In a study by Choi et al.,12 the cutoff point was 150 mm2. Van Bergen et al.14 evaluated the longterm outcome of arthroscopic debridement and bone marrow stimulation for osteochondral defects of the talus and found no correlation between defect size and outcome. Although the Ogilvie-Harris scale score was
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Fig 4. On magnetic resonance imaging, (A) coronal T1-weighted, (B) sagittal T1-weighted, and (C) sagittal fat-suppression sequences show a defect that includes a large cyst located in the medial aspect of the talus (arrows). The arrows in the (D) coronal T1-weighted, (E) sagittal T1-weighted, and (F) sagittal fat-suppression sequences indicate complete filling of the defect and complete integration with the adjacent native cartilage. An intact surface and structure of the repaired tissue are also observed.
excellent in 20% and good in 58% of their patients, no MRI or computed tomography (CT) scan results clearly displayed the defect or cyst characteristics and one-third of the patients progressed to osteoarthritis. The mean diameter of the cysts in our study was 14.47 1.37 mm, and the mean depth was 17.02 1.98 mm. We concluded that large cysts should be filled with grafted tissue to promote healing. One option when using grafts to treat a defect is an osteochondral allograft. An advantage of this option is that the graft is harvested with a specific size, depth, and orientation of curvature that can be matched meticulously to the native talus. Haene et al.5 retrospectively evaluated 16 patients with a mean follow-up period of 4.1 years after fresh bulk osteochondral allograft transplantation for large-volume cystic OCLs of the talus. Failure of graft incorporation occurred in 2 of 16 ankles. Osteolysis, subchondral cysts, and degenerative changes were observed in 5 ankles, 8 ankles, and 7 ankles, respectively. Five ankles were classified as failures, and 2 required a reoperation because of ongoing symptoms. Symptoms persisted in 6 of these patients. Only 4 were ultimately symptom free.5 Because of the high cost, the technically demanding graft preparation process, and clinical evidence, Murawski and Kennedy1 concluded that osteochondral allograft transplantation patients should be chosen carefully to include only those who need salvage procedures or who present with large-volume cystic lesions not amenable to arthroscopic bone marrow stimulation or standard autograft procedures.
The other graft option is autologous osteochondral transplantation from the ipsilateral knee. There are many factors affecting the outcome; for instance, the study by Park and colleagues15 showed that the articular surface of the tibial plafond at the malleolar osteotomy site, soft-tissue impingement, and uncovered areas around the graft were factors affecting the outcome. The advantages of this approach include the viable hyaline cartilage used to replace the defect and the avoidance of a 2-stage procedure, as is the case for osteochondral allograft or chondrocyte transplantation. Reddy et al.6 evaluated graft harvests from asymptomatic knees in 11 patients with a mean follow-up period of 47 months. According to the Lysholm criteria, 5 knees were rated as excellent, 2 as good, and 4 as poor. Knee instability during daily activities was the most common problem. One patient had pain and patellar instability after osteochondral harvest by lateral arthrotomy and required a subsequent lateral retinacular release and tibial tubercle osteotomy. Mosaicplasty is one form of autologous osteochondral transplantation and consists of multiple circular plugs. Apart from the complexity of this procedure and others like it, donor-site morbidity is the most important concern. Espregueira-Mendes et al.16 used autografts from the upper tibiofibular joint to treat knee cartilage lesions and found the grafts effective for treating osteochondral defects in the knee joint; moreover, no relevant complications related to the donor zone were registered. However, to our knowledge, no study has reported the clinical outcome of this technique to treat ankle OCLs.
LARGE CYSTIC MEDIAL OSTEOCHONDRAL LESIONS
Autologous chondrocyte implantation is another option. In principle, the primary advantage of autologous chondrocyte implantation is that it involves transplanting viable, cultured chondrocytes into the defect. Despite promising results with the autologous chondrocyte implantation technique,4,9,14,17-21 patients should be thoroughly counseled regarding the requirement for a 2-stage procedure and other potential risk factors, such as those associated with periosteal harvesting. Many studies have reported that after periosteal graft transplantation, the defect surfaces exhibit chondrogenesis.22-28 Hu et al.3 used autologous osteoperiosteal cylinder grafts from the ipsilateral iliac crest to repair these defects and reported a good clinical outcome, and second-look arthroscopy showed that the lesions were covered with “cartilage-like tissue.” The results were encouraging, but the technique obviously required a graft to be taken from a remote location (i.e., iliac crest) and the graft surface was rough. Therefore, on the basis of the mosaicplasty technique, with good results of animal experiments that used periosteal graft to treat cartilage defects and autologous osteoperiosteal graft from the iliac crest to treat medial OCLs of the talus, we developed the technique of harvesting the graft from the medial tibia to treat OCLs. We had successfully treated 2 patients with this procedure before the initiation of this study. This technique offers an important advantage: The surgical procedure for obtaining and transplanting the graft is performed in the same operative field, minimizing the number of incisions during the operation. Furthermore, the graft surface is smoother than that from the iliac crest. Compared with osteochondral allograft transplantation, autologous osteoperiosteal grafts are less expensive and require a simpler graft preparation. Moreover, no graft incorporation failures, osteolysis, or degenerative changes were observed in this study, confirming the graft viability. Compared with autologous osteochondral transplantation, autologous osteoperiosteal graft exhibits a low rate of donor-site morbidity. Limitations There are several limitations to our study. First, the sample size was relatively small. Second, no secondlook arthroscopy or histologic analysis was performed. Third, CT would have given us a more accurate preoperative size assessment and aided in the postoperative evaluation of bony healing, but in this study, not all patients underwent a CT scan. Consequently, the CT scan results are not presented in this article. Moreover, the intraobserver and interobserver error was not measured. Finally, the AOFAS score has not been validated, and its use is no longer recommended by the AOFAS itself. Thus additional high-level
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evidence, along with histologic and biomechanical studies, is needed.
Conclusions An autologous osteoperiosteal cylinder graft from the medial tibia is effective for treating large cystic medial OCLs of the talus and has a low rate of complications.
References 1. Murawski CD, Kennedy JG. Operative treatment of osteochondral lesions of the talus. J Bone Joint Surg Am 2013;95:1045-1054. 2. Baltzer AW, Arnold JP. Bone-cartilage transplantation from the ipsilateral knee for chondral lesions of the talus. Arthroscopy 2005;21:159-166. 3. Hu Y, Guo Q, Jiao C, et al. Treatment of large cystic medial osteochondral lesions of the talus with autologous osteoperiosteal cylinder grafts. Arthroscopy 2013;29:1372-1379. 4. Tanaka Y, Omokawa S, Fujii T, Kumai T, Sugimoto K, Takakura Y. Vascularized bone graft from the medial calcaneus for treatment of large osteochondral lesions of the medial talus. Foot Ankle Int 2006;27:1143-1147. 5. Haene R, Qamirani E, Story RA, Pinsker E, Daniels TR. Intermediate outcomes of fresh talar osteochondral allografts for treatment of large osteochondral lesions of the talus. J Bone Joint Surg Am 2012;94:1105-1110. 6. Reddy S, Pedowitz DI, Parekh SG, Sennett BJ, Okereke E. The morbidity associated with osteochondral harvest from asymptomatic knees for the treatment of osteochondral lesions of the talus. Am J Sports Med 2007;35:80-85. 7. Kumai T, Takakura Y, Higashiyama I, Tamai S. Arthroscopic drilling for the treatment of osteochondral lesions of the talus. J Bone Joint Surg Am 1999;81:1229-1235. 8. Hunt SA, Sherman O. Arthroscopic treatment of osteochondral lesions of the talus with correlation of outcome scoring systems. Arthroscopy 2003;19:360-367. 9. Robinson DE, Winson IG, Harries WJ, Kelly AJ. Arthroscopic treatment of osteochondral lesions of the talus. J Bone Joint Surg Br 2003;85:989-993. 10. Chuckpaiwong B, Berkson EM, Theodore GH. Microfracture for osteochondral lesions of the ankle: Outcome analysis and outcome predictors of 105 cases. Arthroscopy 2008;24:106-112. 11. Ferkel RD, Zanotti RM, Komenda GA, et al. Arthroscopic treatment of chronic osteochondral lesions of the talus: Long-term results. Am J Sports Med 2008;36:1750-1762. 12. Choi WJ, Park KK, Kim BS, Lee JW. Osteochondral lesion of the talus is there a critical defect size for poor outcome? Am J Sport Med 2009;37:1974-1980. 13. Becher C, Driessen A, Hess T, Longo UG, Maffulli N, Thermann H. Microfracture for chondral defects of the talus: Maintenance of early results at midterm follow-up. Knee Surg Sport Traumatol Arthrosc 2010;18:656-663. 14. van Bergen CJ, Kox LS, Maas M, Sierevelt IN, Kerkhoffs GM, van Dijk CN. Arthroscopic treatment of osteochondral defects of the talus: Outcomes at eight to twenty years of follow-up. J Bone Joint Surg Am 2013;95: 519-525. 15. Kim YS, Park EH, Kim YC, Koh YG, Lee JW. Factors associated with the clinical outcomes of the osteochondral
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W. CHEN ET AL. autograft transfer system in osteochondral lesions of the talus: Second-look arthroscopic evaluation. Am J Sports Med 2012;40:2709-2719. Espregueira-Mendes J, Pereira H, Sevivas N, et al. Osteochondral transplantation using autografts from the upper tibio-fibular joint for the treatment of knee cartilage lesions. Knee Surg Sport Traumatol Arthrosc 2012;20:1136-1142. van Dijk CN, Reilingh ML, Zengerink M, van Bergen CJ. Osteochondral defects in the ankle: Why painful? Knee Surg Sports Traumatol Arthrosc 2010;18:570-580. Giannini S, Buda R, Grigolo B, Vannini F. Autologous chondrocyte transplantation in osteochondral lesions of the ankle joint. Foot Ankle Int 2001;22:513-517. Giannini S, Buda R, Vannini F, Di Caprio F, Grigolo B. Arthroscopic autologous chondrocyte implantation in osteochondral lesions of the talus: Surgical technique and results. Am J Sports Med 2008;36:873-880. Quirbach S, Trattnig S, Marlovits S, et al. Initial results of in vivo high-resolution morphological and biochemical cartilage imaging of patients after matrix-associated autologous chondrocyte transplantation (MACT) of the ankle. Skeletal Radiol 2009;38:751-760. Battaglia M, Vannini F, Buda R, et al. Arthroscopic autologous chondrocyte implantation in osteochondral lesions of the talus: Mid-term T2-mapping MRI evaluation. Knee Surg Sports Traumatol Arthrosc 2011;19: 1376-1384. Ulutas K, Menderes A, Karaca C, Ozkal S. Repair of cartilage defects with periosteal grafts. Br J Plast Surg 2005;58:65-72.
23. Hsieh PC, Thanapipatsiri S, Anderson PC, Wang GJ, Balian G. Repair of full-thickness cartilage defects in rabbit knees with free periosteal graft preincubated with transforming growth factor. Orthopedics 2003;26: 393-402. 24. Rubak JM, Poussa M, Ritsila V. Chondrogenesis in repair of articular cartilage defects by free periosteal grafts in rabbits. Acta Orthop Scand 1982;53:181-186. 25. Shinomiya R, Ochi M, Adachi N, Hachisuka H, Natsu K, Yasunaga Y. The cellular origin of cartilage-like tissue after periosteal transplantation of full-thickness articular cartilage defects: An experimental study using transgenic rats expressing green fluorescent protein. Acta Orthop 2005;76: 920-926. 26. O’Driscoll SW, Keeley FW, Salter RB. Durability of regenerated articular cartilage produced by free autogenous periosteal grafts in major full-thickness defects in joint surfaces under the influence of continuous passive motion. A follow-up report at one year. J Bone Joint Surg Am 1988;70:595-606. 27. Moran ME, Kim HK, Salter RB. Biological resurfacing of full-thickness defects in patellar articular cartilage of the rabbit. Investigation of autogenous periosteal grafts subjected to continuous passive motion. J Bone Joint Surg Br 1992;74:659-667. 28. Lubiatowski P, Manikowski W, Romanowski L, Trzeciak T, Kruczynski J, Piontek T. The experimental reconstruction of articular cartilage using autogenous periosteal and perichondreal implants. Ortop Traumatol Rehabil 2001;3:194-199.
Intermediate Results of Large Cystic Medial Osteochondral Lesions of the Talus Treated With Osteoperiosteal Cylinder Autografts From the Medial Tibia Wan Chen, Ph.D., Kanglai Tang, M.D., Ph.D., Chengsong Yuan, M.D., You Zhou, Ph.D., and Xu Tao, M.D.
Purpose: To investigate the clinical and radiologic outcomes of an autologous osteoperiosteal cylinder graft from the medial tibia for the treatment of large cystic medial osteochondral lesions (OCLs) of the talus. Methods: The study included 15 patients with large cystic medial OCLs. All underwent medial malleolus osteotomy and excision and curettage of the defect site, followed by transplantation with an autologous osteoperiosteal cylinder graft from the medial tibia. They were evaluated preoperatively and after a minimum of 24 months (mean, 44.8 months; range, 24 to 72 months) postoperatively by a visual analog scale, the American Orthopaedic Foot & Ankle Society ankle-hindfoot scale, the OgilvieHarris scale, and magnetic resonance imaging of the ankle. Results: The mean visual analog scale score decreased from 5.40 1.06 points to 1.00 1.00 points (P < .001), and the mean American Orthopaedic Foot & Ankle Society score increased from 49.00 8.96 points to 89.00 4.17 points (P < .001). The mean Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART) score was 64.00 5.07 points. According to the Ogilvie-Harris scale, 7 cases were rated as excellent, 5 as good, 3 as fair, and 0 as poor. No complications were observed. Conclusions: An autologous osteoperiosteal cylinder graft from the medial tibia is effective for treating large cystic medial OCLs of the talus and has a low rate of complications. Level of Evidence: Level IV, case series.
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arge cystic osteochondral lesions (OCLs) of the talus pose a treatment challenge because drilling or debridement alone cannot treat the structural bony defect or restore subchondral support. Graft implantation offers the advantage of restoring the bony integrity. Current options for graft treatment of large cystic medial OCLs of the talus include osteochondral allograft transplantation,1 autologous osteochondral transplantation,2 chondrocyte transplantation, and other grafts from the autologous iliac crest3 and medial calcaneus.4 However, all of these options have disadvantages, such as a high rate of graft incorporation
From the Department of Orthopaedic Surgery, Southwest Hospital, Third Military Medical University, Chongqing, China. The authors report that they have no conflicts of interest in the authorship and publication of this article. Received July 10, 2014; accepted February 19, 2015. Address correspondence to Kanglai Tang, M.D., Ph.D., Department of Orthopaedic Surgery, Southwest Hospital, Third Military Medical University, Chongqing 400038, China. E-mail: [email protected] Ó 2015 by the Arthroscopy Association of North America 0749-8063/14582/$36.00 http://dx.doi.org/10.1016/j.arthro.2015.02.027
failure,1,5 high cost, donor-site morbidity,6 necessity for a 2-stage procedure, and the technically demanding process of graft preparation.1 Recently, we developed a novel technique involving an autologous osteoperiosteal cylinder graft from the medial tibia to repair a large cystic medial OCL of the talus. By comparing postoperative symptom relief, functional improvement, cartilage repair (based on magnetic resonance imaging [MRI]), and complications, this study aimed to investigate the clinical and radiologic outcomes of autologous osteoperiosteal cylinder grafts from the medial tibia used to treat large cystic medial OCLs of the talus. We hypothesized that this novel technique for treating large cystic medial OCLs of the talus using autologous osteoperiosteal cylinder grafts from the medial tibia would result in reduced pain levels, improved function, and improved appearance on MRI.
Methods Patients and Study Design A prospective clinical study was designed. The inclusion criteria for patients consisted of the following: a
Arthroscopy: The Journal of Arthroscopic and Related Surgery, Vol
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Table 1. Patient Details Defect Size Case No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Age, yr 34 55 34 27 32 33 25 46 52 51 49 43 37 34 51
Sex F M M M M M M F M M M F F M M
Side R R R L L R R L R R L R R R R
Diameter, mm, Depth, mm 14.01 14.62 13.43 18.54 11.24 18.26 15.67 19.37 14.44 18.85 15.61 17.99 16.03 18.69 14.77 16.07 14.84 17.87 14.52 18.29 15.44 18.64 12.38 14.67 13.45 15.44 15.87 13.56 15.32 14.39
Volume, mm3 2,252.648 2,625.013 1,810.936 3,733.682 3,085.428 3,441.174 3,770.04 2,751.988 3,089.314 3,027.029 3,488.271 1,764.985 2,192.611 2,680.916 2,651.234
Follow-up Time, mo 36 36 72 60 48 60 48 48 36 36 60 36 48 24 24
NOTE. Volume ¼ p (Diameter/2)2 Depth. F, Female; L, left; M, male; R, right.
type V OCL according to the Scranton and McDermott classification system; an OCL located in the medial talus; and failure to respond to nonoperative treatment (rest, immobilization, anti-inflammatory medication, or physical therapy) for at least 6 months. The exclusion criteria consisted of the following: age younger than 14 years or older than 60 years; presence of osteoporosis; presence of osteoarthritis, rheumatoid arthritis, arthrolithiasis, or related conditions; and presence of a lower limb malalignment. Between October 2008 and February 2012, 15 patients (11 men and 4 women; age range, 25 to 55 years; mean age, 40.2 years; 4 left and 11 right ankles) with large cystic medial OCLs of the talus were included in this prospective clinical and radiologic study. The demographic data, defect size, and follow-up time of each patient were recorded (Table 1). All patients reported ankle pain, and 5 patients reported a history of ankle sprain. The preoperative radiographs showed no other injury, and MRI showed large cystic medial OCLs of the talus. The operation and clinical follow-up were conducted by 2 senior surgeons (K.T., X.T.). The diameter of each cyst was measured on coronal, sagittal, and axial MRI scans, and the largest diameter measured for each cyst was considered. The depth of each cyst was measured on coronal and sagittal MRI scans, and the largest depth measured for each cyst was considered (Fig 1). The study was approved by the Clinical Academic Committee of the Third Military Medical University Southwest Hospital. Surgical Techniques After induction with combined spinal and epidural anesthesia, each patient was placed in the supine position with a tourniquet on the affected thigh (Video 1, available at www.arthroscopyjournal.org). A 10-cm curved longitudinal incision was made over the
medial malleolus. The medial malleolus was exposed by retracting the skin and separating the subcutaneous tissue. Two Kirschner wires were predrilled from the tip of the medial malleolus to the proximal tibia for medial malleolus fixation after osteotomy (Fig 2A). After extraction of the Kirschner wires, the osteotomy orientation of the lateral plane and anteroposterior plane was determined by fluoroscopy. An oblique osteotomy was performed with a microsagittal saw. The osteotomized medial malleolus was then reflected plantarward on the deltoid ligament to expose the medial aspect of the talar dome. The talar dome was inspected to identify the soft point (the cystic lesion surface) by probing. One Kirschner wire was drilled into the middle of the soft point, and a cannulated drill was used to create a small bone socket. The diameter and depth of the recipient socket were determined by MRI before the operation. In addition, all necrotic sequestra and tissue were curetted until bloody marrow oozed from the bone (Fig 2B). The donor site was determined at a location approximately 1.5 cm above the osteotomy plane. At a location approximately 1.5 cm above the osteotomy plus the diameter of the defect, one Kirschner wire was vertically drilled into the tibia. Before use of a trephine with a diameter 1 mm larger than the one used to drill a socket in the talar dome, the periosteum around the trephine apex was incised to avoid damaging the periosteum. The length of the osteoperiosteal cylinder graft harvested from the tibia by the trephine was 1 mm longer than the depth of the socket in the talar dome (Fig 2C). When the graft diameter was larger than 1.5 cm, an allograft was necessary to backfill the donor site.
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LARGE CYSTIC MEDIAL OSTEOCHONDRAL LESIONS
Fig 1. Magnetic resonance imaging scans of cystic osteochondral lesion of talus. The osteochondral lesion is located in the medial talus, and the subchondral cyst is surrounded by bone edema. The cyst measurements are as follows: (A) diameter of 12.02 mm and depth of 15.65 mm on the sagittal image, (B) diameter of 8.89 mm and depth of 16.07 mm on the coronal image, and (C) diameter of 14.77 mm on the axial image. The magnetic resonance imaging scans were measured using a picture archiving and communication system, and the diameter and depth are 14.77 mm and 16.07 mm, respectively. (A, anterior; FL, left foot; FA, anterior view of the foot.)
The graft was inserted into the bone socket of the talus (Fig 2D), and the graft stability was confirmed. Two Kirschner wires were placed into the hole of the medial malleolus, and the osteotomized medial malleolus was reduced. Two cannulated screws (General Care, Shanghai, China) were driven from the tip of the medial malleolus into the cancellous bone of the tibia. The anatomic reduction was confirmed by fluoroscopy. The wounds were closed in a routine manner, and sterile compression dressings were applied. Rehabilitation The postoperative regimen included noneweightbearing activity for 12 weeks. Weight-bearing activity was allowed after clinical and radiologic confirmation of solid union of the osteotomy. Screw extraction was performed after a minimum of 1 year. Clinical Evaluation We used a standard 10-point visual analog scale (VAS) and the American Orthopaedic Foot & Ankle Society (AOFAS) ankle-hindfoot scale to evaluate the symptoms and functional level of each patient before and a minimum of 24 months after surgery. All patients received an MRI scan before and a minimum of 24 months after surgery. The MRI parameters were as follows: repetition time, 600 milliseconds; echo time, 26 milliseconds; field of view, 180 160 mm; thickness, 3 mm; matrix, 192 128; and scanner tesla rating, 0.2 T. In addition, 2 musculoskeletal radiologists independently used the Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART) scoring system to evaluate the degree of defect repair and the integrity of
the subchondral bone at a minimum of 24 months after surgery. There were no significant differences between the 2 radiologists’ results. The mean score was used as the final score. The results of the operation were evaluated using the Ogilvie-Harris scale score for pain, swelling, stiffness, limping, and activity and were categorized as excellent, good, fair, or poor. For each patient, the lowest value among the individual categories was used as the final score. Statistical analysis was performed using SPSS software, version 13.0 (IBM, Armonk, NY). Paired-samples t tests and the Mann-Whitney U test were used to compare the VAS scores and AOFAS scores, respectively, before and after the procedures. The level of significance was set at 95%; P < .05 was considered significant.
Results According to the previously described criteria, 27 patients with noncystic OCLs, 6 with lateral OCLs, 8 with lateral noncystic OCLs, 17 with large medial cystic OCLs with osteoarthritis, and 2 with large medial cystic OCLs with lower limb malalignment were excluded, whereas 15 patients were included and treated with autologous osteoperiosteal cylinder grafts from the medial tibia. The mean time of follow-up was 44.8 months (range, 24 to 72 months). No patients were lost to follow-up. The mean VAS score improved from 5.40 1.06 points preoperatively to 1.00 1.00 points 2 years postoperatively (P < .001). The mean AOFAS score improved from 49.00 8.96 points preoperatively to 89.00 4.17 points 2 years postoperatively
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Fig 2. Graft harvest technique in a left foot. (A) Two Kirschner wires were predrilled for medial malleolus fixation after osteotomy. (B) A cannulated drill was used to create a small bone socket. (C) A trephine with a diameter larger than the one used to create a socket in the talar dome was used to drill into the tibia and harvest the osteoperiosteal cylinder graft. (D) The graft was inserted into the bone socket of the talus.
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LARGE CYSTIC MEDIAL OSTEOCHONDRAL LESIONS Table 2. Clinical Evaluation of Patients VAS Score Case No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Mean Total
AOFAS Score
Preoperative
Postoperative
Preoperative
Postoperative
MOCART Score
Ogilvie-Harris Scale Score
7 6 5 5 7 4 6 5 5 4 7 4 6 5 5 5.40 1.06 81
3 2 0 0 0 1 1 0 2 0 2 0 2 1 1 1.00 1.00 15
40 42 47 46 40 59 41 45 65 58 40 57 40 60 55 49.00 8.96 735
80 83 93 90 90 90 86 95 85 91 87 95 90 90 90 89.00 4.17 1,335
55 55 70 65 65 65 60 70 60 70 60 70 65 65 65 64.00 5.07 1,024
Fair Fair Excellent Excellent Good Excellent Good Excellent Fair Excellent Good Excellent Good Good Excellent
NOTE. For each patient, the lowest item of the Ogilvie-Harris score determines the final score. AOFAS, American Orthopaedic Foot & Ankle Society; MOCART, Magnetic Resonance Observation of Cartilage Repair Tissue; VAS, visual analog scale.
(P < .001) (Table 2, Fig 3). The mean Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART) score was 64.00 5.07 points. On the basis of the Ogilvie-Harris scale, 7 cases were rated as excellent, 5 as good, 3 as fair, and 0 as poor (Table 2). After 2 years, all MRI scans showed complete filling of the defects and complete integration with the adjacent native cartilage, as well as an intact surface and structure of the repaired tissue (Fig 4). No complications were observed.
Discussion Our results showed that autologous osteoperiosteal cylinder grafts from the medial tibia were an effective treatment for large cystic medial OCLs of the talus, resulting in pain relief, functional improvement, and
Fig 3. After the operation, the visual analog scale (VAS) score significantly decreased (P < .001) in 11 patients and the American Orthopaedic Foot & Ankle Society (AOFAS) score significantly increased (P < .001) in all 15 patients.
incorporation of the grafts and complete filling of the defects. Osteochondral defects with small subchondral cysts can be treated effectively with arthroscopic microfracture or abrasion arthroplasty, so definition of “large cystic” is a cutoff for an OCL size that is not fit for microfracture or other conservative treatment. Many studies have shown that the defect size is a significant predictor of outcome.7-13 In a study of lesions smaller than 15 mm by Chuckpaiwong et al.,10 excellent results were obtained in response to microfracture for OCLs of the ankle. In a study by Choi et al.,12 the cutoff point was 150 mm2. Van Bergen et al.14 evaluated the longterm outcome of arthroscopic debridement and bone marrow stimulation for osteochondral defects of the talus and found no correlation between defect size and outcome. Although the Ogilvie-Harris scale score was
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Fig 4. On magnetic resonance imaging, (A) coronal T1-weighted, (B) sagittal T1-weighted, and (C) sagittal fat-suppression sequences show a defect that includes a large cyst located in the medial aspect of the talus (arrows). The arrows in the (D) coronal T1-weighted, (E) sagittal T1-weighted, and (F) sagittal fat-suppression sequences indicate complete filling of the defect and complete integration with the adjacent native cartilage. An intact surface and structure of the repaired tissue are also observed.
excellent in 20% and good in 58% of their patients, no MRI or computed tomography (CT) scan results clearly displayed the defect or cyst characteristics and one-third of the patients progressed to osteoarthritis. The mean diameter of the cysts in our study was 14.47 1.37 mm, and the mean depth was 17.02 1.98 mm. We concluded that large cysts should be filled with grafted tissue to promote healing. One option when using grafts to treat a defect is an osteochondral allograft. An advantage of this option is that the graft is harvested with a specific size, depth, and orientation of curvature that can be matched meticulously to the native talus. Haene et al.5 retrospectively evaluated 16 patients with a mean follow-up period of 4.1 years after fresh bulk osteochondral allograft transplantation for large-volume cystic OCLs of the talus. Failure of graft incorporation occurred in 2 of 16 ankles. Osteolysis, subchondral cysts, and degenerative changes were observed in 5 ankles, 8 ankles, and 7 ankles, respectively. Five ankles were classified as failures, and 2 required a reoperation because of ongoing symptoms. Symptoms persisted in 6 of these patients. Only 4 were ultimately symptom free.5 Because of the high cost, the technically demanding graft preparation process, and clinical evidence, Murawski and Kennedy1 concluded that osteochondral allograft transplantation patients should be chosen carefully to include only those who need salvage procedures or who present with large-volume cystic lesions not amenable to arthroscopic bone marrow stimulation or standard autograft procedures.
The other graft option is autologous osteochondral transplantation from the ipsilateral knee. There are many factors affecting the outcome; for instance, the study by Park and colleagues15 showed that the articular surface of the tibial plafond at the malleolar osteotomy site, soft-tissue impingement, and uncovered areas around the graft were factors affecting the outcome. The advantages of this approach include the viable hyaline cartilage used to replace the defect and the avoidance of a 2-stage procedure, as is the case for osteochondral allograft or chondrocyte transplantation. Reddy et al.6 evaluated graft harvests from asymptomatic knees in 11 patients with a mean follow-up period of 47 months. According to the Lysholm criteria, 5 knees were rated as excellent, 2 as good, and 4 as poor. Knee instability during daily activities was the most common problem. One patient had pain and patellar instability after osteochondral harvest by lateral arthrotomy and required a subsequent lateral retinacular release and tibial tubercle osteotomy. Mosaicplasty is one form of autologous osteochondral transplantation and consists of multiple circular plugs. Apart from the complexity of this procedure and others like it, donor-site morbidity is the most important concern. Espregueira-Mendes et al.16 used autografts from the upper tibiofibular joint to treat knee cartilage lesions and found the grafts effective for treating osteochondral defects in the knee joint; moreover, no relevant complications related to the donor zone were registered. However, to our knowledge, no study has reported the clinical outcome of this technique to treat ankle OCLs.
LARGE CYSTIC MEDIAL OSTEOCHONDRAL LESIONS
Autologous chondrocyte implantation is another option. In principle, the primary advantage of autologous chondrocyte implantation is that it involves transplanting viable, cultured chondrocytes into the defect. Despite promising results with the autologous chondrocyte implantation technique,4,9,14,17-21 patients should be thoroughly counseled regarding the requirement for a 2-stage procedure and other potential risk factors, such as those associated with periosteal harvesting. Many studies have reported that after periosteal graft transplantation, the defect surfaces exhibit chondrogenesis.22-28 Hu et al.3 used autologous osteoperiosteal cylinder grafts from the ipsilateral iliac crest to repair these defects and reported a good clinical outcome, and second-look arthroscopy showed that the lesions were covered with “cartilage-like tissue.” The results were encouraging, but the technique obviously required a graft to be taken from a remote location (i.e., iliac crest) and the graft surface was rough. Therefore, on the basis of the mosaicplasty technique, with good results of animal experiments that used periosteal graft to treat cartilage defects and autologous osteoperiosteal graft from the iliac crest to treat medial OCLs of the talus, we developed the technique of harvesting the graft from the medial tibia to treat OCLs. We had successfully treated 2 patients with this procedure before the initiation of this study. This technique offers an important advantage: The surgical procedure for obtaining and transplanting the graft is performed in the same operative field, minimizing the number of incisions during the operation. Furthermore, the graft surface is smoother than that from the iliac crest. Compared with osteochondral allograft transplantation, autologous osteoperiosteal grafts are less expensive and require a simpler graft preparation. Moreover, no graft incorporation failures, osteolysis, or degenerative changes were observed in this study, confirming the graft viability. Compared with autologous osteochondral transplantation, autologous osteoperiosteal graft exhibits a low rate of donor-site morbidity. Limitations There are several limitations to our study. First, the sample size was relatively small. Second, no secondlook arthroscopy or histologic analysis was performed. Third, CT would have given us a more accurate preoperative size assessment and aided in the postoperative evaluation of bony healing, but in this study, not all patients underwent a CT scan. Consequently, the CT scan results are not presented in this article. Moreover, the intraobserver and interobserver error was not measured. Finally, the AOFAS score has not been validated, and its use is no longer recommended by the AOFAS itself. Thus additional high-level
7
evidence, along with histologic and biomechanical studies, is needed.
Conclusions An autologous osteoperiosteal cylinder graft from the medial tibia is effective for treating large cystic medial OCLs of the talus and has a low rate of complications.
References 1. Murawski CD, Kennedy JG. Operative treatment of osteochondral lesions of the talus. J Bone Joint Surg Am 2013;95:1045-1054. 2. Baltzer AW, Arnold JP. Bone-cartilage transplantation from the ipsilateral knee for chondral lesions of the talus. Arthroscopy 2005;21:159-166. 3. Hu Y, Guo Q, Jiao C, et al. Treatment of large cystic medial osteochondral lesions of the talus with autologous osteoperiosteal cylinder grafts. Arthroscopy 2013;29:1372-1379. 4. Tanaka Y, Omokawa S, Fujii T, Kumai T, Sugimoto K, Takakura Y. Vascularized bone graft from the medial calcaneus for treatment of large osteochondral lesions of the medial talus. Foot Ankle Int 2006;27:1143-1147. 5. Haene R, Qamirani E, Story RA, Pinsker E, Daniels TR. Intermediate outcomes of fresh talar osteochondral allografts for treatment of large osteochondral lesions of the talus. J Bone Joint Surg Am 2012;94:1105-1110. 6. Reddy S, Pedowitz DI, Parekh SG, Sennett BJ, Okereke E. The morbidity associated with osteochondral harvest from asymptomatic knees for the treatment of osteochondral lesions of the talus. Am J Sports Med 2007;35:80-85. 7. Kumai T, Takakura Y, Higashiyama I, Tamai S. Arthroscopic drilling for the treatment of osteochondral lesions of the talus. J Bone Joint Surg Am 1999;81:1229-1235. 8. Hunt SA, Sherman O. Arthroscopic treatment of osteochondral lesions of the talus with correlation of outcome scoring systems. Arthroscopy 2003;19:360-367. 9. Robinson DE, Winson IG, Harries WJ, Kelly AJ. Arthroscopic treatment of osteochondral lesions of the talus. J Bone Joint Surg Br 2003;85:989-993. 10. Chuckpaiwong B, Berkson EM, Theodore GH. Microfracture for osteochondral lesions of the ankle: Outcome analysis and outcome predictors of 105 cases. Arthroscopy 2008;24:106-112. 11. Ferkel RD, Zanotti RM, Komenda GA, et al. Arthroscopic treatment of chronic osteochondral lesions of the talus: Long-term results. Am J Sports Med 2008;36:1750-1762. 12. Choi WJ, Park KK, Kim BS, Lee JW. Osteochondral lesion of the talus is there a critical defect size for poor outcome? Am J Sport Med 2009;37:1974-1980. 13. Becher C, Driessen A, Hess T, Longo UG, Maffulli N, Thermann H. Microfracture for chondral defects of the talus: Maintenance of early results at midterm follow-up. Knee Surg Sport Traumatol Arthrosc 2010;18:656-663. 14. van Bergen CJ, Kox LS, Maas M, Sierevelt IN, Kerkhoffs GM, van Dijk CN. Arthroscopic treatment of osteochondral defects of the talus: Outcomes at eight to twenty years of follow-up. J Bone Joint Surg Am 2013;95: 519-525. 15. Kim YS, Park EH, Kim YC, Koh YG, Lee JW. Factors associated with the clinical outcomes of the osteochondral
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W. CHEN ET AL. autograft transfer system in osteochondral lesions of the talus: Second-look arthroscopic evaluation. Am J Sports Med 2012;40:2709-2719. Espregueira-Mendes J, Pereira H, Sevivas N, et al. Osteochondral transplantation using autografts from the upper tibio-fibular joint for the treatment of knee cartilage lesions. Knee Surg Sport Traumatol Arthrosc 2012;20:1136-1142. van Dijk CN, Reilingh ML, Zengerink M, van Bergen CJ. Osteochondral defects in the ankle: Why painful? Knee Surg Sports Traumatol Arthrosc 2010;18:570-580. Giannini S, Buda R, Grigolo B, Vannini F. Autologous chondrocyte transplantation in osteochondral lesions of the ankle joint. Foot Ankle Int 2001;22:513-517. Giannini S, Buda R, Vannini F, Di Caprio F, Grigolo B. Arthroscopic autologous chondrocyte implantation in osteochondral lesions of the talus: Surgical technique and results. Am J Sports Med 2008;36:873-880. Quirbach S, Trattnig S, Marlovits S, et al. Initial results of in vivo high-resolution morphological and biochemical cartilage imaging of patients after matrix-associated autologous chondrocyte transplantation (MACT) of the ankle. Skeletal Radiol 2009;38:751-760. Battaglia M, Vannini F, Buda R, et al. Arthroscopic autologous chondrocyte implantation in osteochondral lesions of the talus: Mid-term T2-mapping MRI evaluation. Knee Surg Sports Traumatol Arthrosc 2011;19: 1376-1384. Ulutas K, Menderes A, Karaca C, Ozkal S. Repair of cartilage defects with periosteal grafts. Br J Plast Surg 2005;58:65-72.
23. Hsieh PC, Thanapipatsiri S, Anderson PC, Wang GJ, Balian G. Repair of full-thickness cartilage defects in rabbit knees with free periosteal graft preincubated with transforming growth factor. Orthopedics 2003;26: 393-402. 24. Rubak JM, Poussa M, Ritsila V. Chondrogenesis in repair of articular cartilage defects by free periosteal grafts in rabbits. Acta Orthop Scand 1982;53:181-186. 25. Shinomiya R, Ochi M, Adachi N, Hachisuka H, Natsu K, Yasunaga Y. The cellular origin of cartilage-like tissue after periosteal transplantation of full-thickness articular cartilage defects: An experimental study using transgenic rats expressing green fluorescent protein. Acta Orthop 2005;76: 920-926. 26. O’Driscoll SW, Keeley FW, Salter RB. Durability of regenerated articular cartilage produced by free autogenous periosteal grafts in major full-thickness defects in joint surfaces under the influence of continuous passive motion. A follow-up report at one year. J Bone Joint Surg Am 1988;70:595-606. 27. Moran ME, Kim HK, Salter RB. Biological resurfacing of full-thickness defects in patellar articular cartilage of the rabbit. Investigation of autogenous periosteal grafts subjected to continuous passive motion. J Bone Joint Surg Br 1992;74:659-667. 28. Lubiatowski P, Manikowski W, Romanowski L, Trzeciak T, Kruczynski J, Piontek T. The experimental reconstruction of articular cartilage using autogenous periosteal and perichondreal implants. Ortop Traumatol Rehabil 2001;3:194-199.