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High density-autologous chondrocyte implantation for the treatment of bilateral ankle cartilage defects: Report of two cases

Open AccessPublished:June 14, 2022DOI:https://doi.org/10.1016/j.fastrc.2022.100218

      Abstract

      Purpose

      To study clinical outcome of patients with bilateral ankle chondral defects treated with High-Density Autologous Chondrocyte Implantation (HD-ACI) in the same surgical act.

      Cases presentation

      Two men (27 and 48 years-old) with chondral defects in both ankles evidenced by MRI. Chondral lesions were treated with HD-ACI in the same surgical act and anesthesia, consecutively. Patients were evaluated 2, 6 and 12 months after surgery to check for treatment safety and efficacy. Pain, evaluated by the Visual Analogic Scale (VAS), decreased from very high values (8.5 – 9) to normal or almost normal scores one year after surgery (0 – 1). Ankle functionality measured by the American Orthopedic Foot & Ankle Society score (AOFAS) and quality of life evaluated by the EuroQol five-dimensional five-level questionnaire (EQ-5D-5L) behaved similarly to pain. Thus, both parameters increased and/or slightly decreased at 2 months (AOFAS score: 53 and 51; EQ-5D-5L score: 0.42 and 0.33) and reached their maximum value at 12 months (AOFAS score: 90 and 89; EQ-5D-5L score: 0.89 and 0.91). MRI from both ankles revealed that chondral defects were filled with a material of similar aspect to the surrounding cartilage.

      Conclusion

      Treatment of both ankles with HD-ACI in the same surgical act in patients with bilateral chondral lesions is a safe procedure, providing positive results from the clinical and patients’ quality of life points of view.

      Keywords

      Introduction

      Osteochondral lesions of the talus (OLT) are focal areas of damaged articular cartilage with injury in the subjacent subchondral bone.
      • Murawski CD
      • Kennedy JG.
      Operative treatment of. osteochondral lesions of the talus.
      Trauma and osteochondritis dissecans have been proposed as the most frequent causes for osteochondral lesions.
      • Wang CC
      • Yang KC
      • Chen IH.
      Current treatment concepts for osteochondral lesions of the talus.
      Bilateral OLTs are relatively uncommon and in most cases are the cause of pain and discomfort.
      • Letts M
      • Davidson D
      • Ahmer A.
      Osteochondritis dissecans of the talus in children.
      ,
      • Hermanson E
      • Ferkel RD.
      Bilateral osteochondral lesions of the talus.
      In current medical practice, cell therapy and regenerative medicine techniques, such as autologous chondrocyte implantation (ACI), are some of the best options to treat OLT.
      • Lan T
      • McCarthy HS
      • Hulme CH
      • Wright KT
      • Makwana N.
      The management of talar osteochondral lesions - Current concepts.
      ACI was first used with the cells in liquid medium implanted under a periosteum flap.
      • Brittberg M
      • Lindahl A
      • Nilsson A
      • Ohlsson C
      • Isaksson O
      • Peterson L.
      Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation.
      In MACI (Matrix-Assisted Chondrocyte Implantation) version, cells were seeded onto a porcine type I/III collagen membrane as a carrier at a density of 1 million cells per cm2, facilitating cell delivery to the chondral defect.
      • Ronga M
      • Grassi FA
      • Manelli A
      • Bulgheroni P.
      Tissue engineering techniques for the treatment of a complex knee injury.
      We developed a modification of MACI technique, called High Density-Autologous Chondrocyte Implantation (HD-ACI), which features a 5-fold increase in the number cells, resulting in 5 million chondrocytes per cm2 of lesion using a porcine type I/III collagen membrane being implanted on the chondral defect. This technique has been successfully used to treat chondral lesions in the knee
      • Lopez-Alcorocho JM
      • Aboli L
      • Guillen-Vicente I
      • Rodriguez-Iñigo E
      • Guillen-Vicente M
      • Fernández-Jaén TF
      • Arauz S
      • Abelow S
      • Guillen-García P.
      Cartilage defect treatment using high-density autologous chondrocyte implantation: two-year follow-up.
      and ankle.
      • López-Alcorocho JM
      • Guillén-Vicente I
      • Rodríguez-Iñigo E
      • Navarro R
      • Caballero-Santos R
      • Guillén-Vicente M
      • Casqueiro M
      • Fernández-Jaén TF
      • Sanz F
      • Arauz S
      • Abelow S
      • Guillén-García P.
      High-density autologous chondrocyte implantation as treatment for ankle osteochondral defects.
      We have recently published satisfactory results on the use of HD-ACI in patients with bilateral knee chondral defects.
      • Guillén-Vicente I
      • López-Alcorocho JM
      • Rodríguez-Iñigo E
      • Guillén-Vicente M
      • Fernández-Jaén TF
      • Cortés JM
      • Abelow S.
      • Guillén-García P.
      High-density autologous chondrocyte implantation (HD-ACI) in patients with bilateral knee chondral defects.
      In this work, we describe the treatment with HD-ACI in the same surgical act in 2 patients with bilateral ankle chondral lesions.

      Cases presentation

      Here we describe the treatment in two male patients (27 and 48 years old) with bilateral ankle cartilage lesions treated with HD-ACI. The study was conducted in accordance to the ethical standards of the Helsinki Declaration of 1964, revised in 2013. Patients included in the study signed an informed consent.
      Patient 1 had an osteochondral lesion of 10 mm × 6 mm in size in the superomedial corner of the talus in the left foot, and a chondral defect of 9 mm × 10 mm in size and bone edema in the superomedial corner of the talus in the right ankle. Patient 2 had an osteochondral lesion of 16 mm × 8 mm in size located in the superomedial corner of the talus in the left foot, together with subchondral cyst and bone edema, and an osteochondral lesion of 14 mm × 6 mm in size of the superomedial corner of the talus in the right ankle. In both cases, cartilage lesions were diagnosed by X-ray and confirmed by magnetic resonance (MRI).
      Patients underwent a first arthroscopy to harvest a cartilage biopsy from the anterior talar neck of one of the ankles. Isolation and culture of cells were carried-out following previously described procedures.
      • Lopez-Alcorocho JM
      • Aboli L
      • Guillen-Vicente I
      • Rodriguez-Iñigo E
      • Guillen-Vicente M
      • Fernández-Jaén TF
      • Arauz S
      • Abelow S
      • Guillen-García P.
      Cartilage defect treatment using high-density autologous chondrocyte implantation: two-year follow-up.
      ,
      • López-Alcorocho JM
      • Guillén-Vicente I
      • Rodríguez-Iñigo E
      • Navarro R
      • Caballero-Santos R
      • Guillén-Vicente M
      • Casqueiro M
      • Fernández-Jaén TF
      • Sanz F
      • Arauz S
      • Abelow S
      • Guillén-García P.
      High-density autologous chondrocyte implantation as treatment for ankle osteochondral defects.
      Chondrocytes loaded in a resorbable porcine type I/III collagen membrane (Chondro-Gide, Geistlich Biomaterials, Wolhusen, Switzerland) were implanted in a second surgery.
      In the same surgical act we successively operated both ankles, under the same anesthesic procedure. Main steps followed during surgery are shown in Fig. 1. As previously described,
      • López-Alcorocho JM
      • Guillén-Vicente I
      • Rodríguez-Iñigo E
      • Navarro R
      • Caballero-Santos R
      • Guillén-Vicente M
      • Casqueiro M
      • Fernández-Jaén TF
      • Sanz F
      • Arauz S
      • Abelow S
      • Guillén-García P.
      High-density autologous chondrocyte implantation as treatment for ankle osteochondral defects.
      in each ankle we first proceeded with a 5 cm longitudinal approach on medial malleolus and once the periosteal plane was reached, anterior and posterior tibial malleolus points were marked. Flexor retinaculum was then accessed and posterior tibial tendon was protected using a separator. To fix bone osteotomy, guide needle positioning and threading then followed prior to tibial osteotomy for both 4.5 mm partial thread malleolar screws (Fig. 1a). Under radioscopy control, perpendicular axis of osteotomy was marked in lesion apex of zone 4 according to Elias classification
      • Elias I
      • Zoga AC
      • Morrison WB
      • Besser MP
      • Schweitzer ME
      • Raikin SM.
      Osteochondral lesions of the talus: localization and morphologic data from 424 patients using a novel anatomical grid scheme.
      and after screws were removed, a cut was made towards the internal cortex. While carefully handling adjacent soft tissues, tibial malleolus was proximally lifted with a bone clamp providing access to lesion. The edges and the bed of osteochondral lesion were debrided, leaving perpendicular edges along its perimeter (Fig. 1b). The membrane was then fixed to the surrounding cartilage using either 5-0 Vicryl resorbable suture or transosseous sutures, followed by fibrin sealant (Fig. 1c). Once forced manual flexion-extension movements confirmed overall stability, X-rays were then performed to confirm all elements had been properly fixed (Fig. 1d).
      Fig. 1
      Fig. 1Main steps followed during high-density autologous chondrocyte implantation (HD-ACI). Before performing the tibial osteotomy, guide needles were positioned and threaded for both 4.5 mm partial thread malleolar screws to fix bone cut (a). After osteotomy, the edges and the bed of the ostechondral lesion were debrided, leaving perpendicular edges along its perimeter (b). Membrane was then fixed to the surrounding cartilage (c). Manual flexion-extension movements were performed to confirm overall stability and X-rays then confirmed all elements had been properly fixed (d).
      Patients then underwent mobilization programme with no weight-bearing from the first week until the 6th – 8th week, followed by 6 – 8 weeks of progressive weight-bearing with crutches which also included the start of physical-therapy sessions. During the 6 – 8 non weight-bearing weeks, patients received DVT (Deep Venous Thrombosis) prophylaxis with 3,500 IU bemiparin injection every 24 hours. At 4 months, patients may also be involved in stationary bicycle sessions and swimming. At 10 – 12 months they were allowed to jog slowly.
      Treatment effectiveness was assessed by evaluating pain using the Visual Analogical Scale (VAS) and American Orthopaedic Foot & Ankle Society (AOFAS) ankle-hindfoot score
      • Cook JJ
      • Cook EA
      • Rosenblum BI
      • Landsman AS
      • Roukis TS.
      Validation of the American College of Foot and Ankle surgeons scoring scales.
      at 2, 6 and 12 months follow-up. EuroQol five-dimensional five-level questionnaire (EQ-5D-5L) and Visual Analogic Scale for health included in the questionnaire were used to evaluate overall health of patients.
      • van Hout B
      • Janssen MF
      • Feng YS
      • Kohlmann T
      • Busschbach J
      • Golicki D
      • Lloyd A
      • Scalone L
      • Kind P
      • Pickard AS.
      Interim scoring for the EQ-5D-5L: mapping the EQ-5D-5L to EQ-5D-3L value sets.
      Patients underwent MRI at 6- and 12- months follow-up. Adverse events including swelling and bone edema were recorded at 3-, 6- and 12-month follow-up to evaluate treatment safety.

      Results

      After chondrocyte implantation neither patient had swelling, bone edema, DVT nor other surgery-derived complications. With respect to pain, as seen in Table 1, both patients had a high pre-op VAS score which slightly decreased at 2 months and dramatically decreased at 6 months to reach almost normal scores at 12 months (Table 1). Evolution of ankle functionality measured by AOFAS and quality of life evaluated by EQ-5D-5L along the study are depicted in Fig. 2. In both patients, both parameters evolved similarly to pain: values increased and/or slightly decreased at 2 months and rapidly increased at 6 months to reach a maximum score at 12 months (Fig. 2). Six- and twelve-month MRIs from both ankles in both patients are shown in Fig. 3. In the 4 ankles, images revealed that chondral defects were filled with a material similar to normal surrounding cartilage. Subchondral cyst evidenced before treatment in patient 2 and bone edema presented in both cases in the baseline were not detected at 12-month follow-up MRI.
      Table 1VAS score in both patients throughout the study
      Baseline2 months6 months12 months
      LeftRightLeftRightLeftRightLeftRight
      Patient 198.58722.511
      Patient 2996.551210
      Fig. 2
      Fig. 2Evolution of AOFAS (A) and EQ-5D-5L (B) questionnaires values along the study. In both patients values increased and/or slightly decreased at 2 months and rapidly increased at 6 months to reach a top score at 12 months.
      Fig. 3
      Fig. 3Patient 1 (a1-d1) and patient 2 (a2-d2) MRIs taken from right (a1, c1, a2, c2) and left (b1, d1, b2, d2) ankles, 6 (a1, b1, a2, b2) and 12 (c1, d1, c2, d2) months after surgery. Images revealed that chondral defects were filled with a material similar to the normal surrounding cartilage. Some artifacts due to screws are evidenced, preventing subchondral cyst and bone edema detection.

      Discussion

      In this work we present two cases of patients with bilateral ankle cartilage chondral defects treated with HD-ACI, whose feet were successively operated in the same surgical act, under the same anesthesia. After 1-year follow-up, clinical outcome and quality of life improved when compared to pre-surgery condition. As described in a previous study conducted on patients with bilateral knee cartilage lesions, the main issue is to decide whether to operate both limbs in the same surgical act or in separate ones.
      • Guillén-Vicente I
      • López-Alcorocho JM
      • Rodríguez-Iñigo E
      • Guillén-Vicente M
      • Fernández-Jaén TF
      • Cortés JM
      • Abelow S.
      • Guillén-García P.
      High-density autologous chondrocyte implantation (HD-ACI) in patients with bilateral knee chondral defects.
      In this previous study, eight patients with bilateral knee chondral defects consecutively treated with HD-ACI, were included. We first explained the pros- and cons- of each option to patients and they decided whether they would like to undergo one or two surgeries.
      • Guillén-Vicente I
      • López-Alcorocho JM
      • Rodríguez-Iñigo E
      • Guillén-Vicente M
      • Fernández-Jaén TF
      • Cortés JM
      • Abelow S.
      • Guillén-García P.
      High-density autologous chondrocyte implantation (HD-ACI) in patients with bilateral knee chondral defects.
      If two surgeries was their choice, after recovering from the first surgery, patients would likely need to spend more time to return to previous activities, due to the burden of those two surgeries, yet on the other hand, these patients may have less mobility issues throughout their recovery time as just that one leg is immobilized after each surgery. If patients’ choice was to undergo one single surgery they only have to recover from one surgery while suffering the inconvenience of having both legs immobilized.
      • Guillén-Vicente I
      • López-Alcorocho JM
      • Rodríguez-Iñigo E
      • Guillén-Vicente M
      • Fernández-Jaén TF
      • Cortés JM
      • Abelow S.
      • Guillén-García P.
      High-density autologous chondrocyte implantation (HD-ACI) in patients with bilateral knee chondral defects.
      In that work we concluded that simultaneous treatment of chondral defects from both limbs with HD-ACI is a safe procedure with good results in terms of clinical outcome and quality of life.
      • Guillén-Vicente I
      • López-Alcorocho JM
      • Rodríguez-Iñigo E
      • Guillén-Vicente M
      • Fernández-Jaén TF
      • Cortés JM
      • Abelow S.
      • Guillén-García P.
      High-density autologous chondrocyte implantation (HD-ACI) in patients with bilateral knee chondral defects.
      Given the good results obtained in the knee we followed the same procedure with cartilage lesions in both ankles and 2 patients accepted to have just one surgery in which one ankle was operated after the other.
      One year after surgery both patients had almost normal values of pain (measured by VAS) and high AOFAS score which indicates a satisfactory clinical outcome in both cases. It is noteworthy that the difference in the AOFAS score compared with the basal one was 3 and -2 at 2 months and increased to 31 and 19 at 6 months, reaching 40 and 36 at 12 months in both cases. It has been published that Minimal Clinically Important Difference in the AOFAS for hallux valgus surgery is 7.9 to 30.2.
      • Chan HY
      • Chen JY
      • Zainul-Abidin S
      • Ying H
      • Koo K
      • Rikhraj IS.
      Minimal clinically important differences for American Orthopaedic Foot & Ankle Society score in hallux valgus surgery.
      Although hallux valgus surgery is a different medical condition than that of our patients, a difference of 40 and 36 at 12 months in our patients may give us the idea that they perceived this as a real improvement. Furthermore, these good clinical outcomes are accompanied by the absence of adverse events, good MRI results and quality of life improvement. It is also worth mentioning that MRI did not reveal the presence of neither bone edema nor bone cyst. However, this result is not conclusive since during surgery two screws were placed to promote osteotomy consolidation and may interfere with magnetic fields in the MRI giving rise to artifacts that can lead to image misinterpretation. Chondrocyte implantation in the ankle implies the need to carry-out a medial malleolus osteotomy to access the chondral lesion and treat it (two osteotomies in bilateral cases). This fact may well influence post-operative rehabilitation and could delay weight-bearing. However, both patients followed the prescribed post-operative program and schedule, showing that bilateral chondral lesion treatment neither influenced post-operative rehabilitation nor delayed weight-bearing.
      Both patients received DVT prophylaxis during the non-weight-bearing period. No thrombotic episodes were observed in either patient, indicating that venous thromboembolism prophylaxis was effective. There are no clear guidelines published about DVT prohylaxis in foot and ankle surgery, due to the wide variety and complexity of injuries and procedures as well as post-operative protocols.
      • Carr P
      • Ehredt Jr, DJ
      • Dawoodian A.
      Prevention of deep venous thromboembolism in foot and ankle surgery.
      The American College of Foot and Ankle Surgeons has published a clinical consensus statement for perioperative management of foot and ankle surgery patients.
      • Meyr AJ
      • Mirmiran R
      • Naldo J
      • Sachs BD
      • Shibuya N.
      American College of Foot and Ankle Surgeons® clinical consensus statement: perioperative management.
      In this document, expert panel concluded that the routine use of pharmacologic antithrombotic prophylaxis may not be necessary in all cases but should be considered for some patients with high risk of venous thromboembolism development. Such a prolonged time of non-weight-bearing (6 – 8 weeks) is a risk factor for DVT which is why we consider that DVT prophylaxis is necessary and, from our experience, leads to satisfactory results.
      Scarce literature about simultaneous surgery on both ankles due to any bilateral lesion has been published. Recently, Gordon et al.
      • Gordon D
      • Crooks SA
      • Lewis TL
      • Ray R.
      Bilateral vs unilateral minimally invasive hallux valgus surgery: a propensity matched case-control study with 2 year clinical patient reported outcomes.
      published a study comparing bilateral vs unilateral minimally invasive surgery for hallux valgus. The study demonstrates that there is no difference in clinical outcome between patients who underwent bilateral versus unilateral surgery. Furthermore, no differences in both clinical and radiological parameters were found between both groups of patients and according to the authors, this finding should encourage surgeons to consider performing bilateral surgery.
      • Gordon D
      • Crooks SA
      • Lewis TL
      • Ray R.
      Bilateral vs unilateral minimally invasive hallux valgus surgery: a propensity matched case-control study with 2 year clinical patient reported outcomes.
      Of course, chondrocyte implantation in the ankle is a more aggressive surgery requiring a longer postoperative recovery period than hallux valgus surgery. However, we decided to offer our patients with bilateral ankle chondral lesions to have a single surgery supported by our results in patients with bilateral knee chondral defects.
      • Guillén-Vicente I
      • López-Alcorocho JM
      • Rodríguez-Iñigo E
      • Guillén-Vicente M
      • Fernández-Jaén TF
      • Cortés JM
      • Abelow S.
      • Guillén-García P.
      High-density autologous chondrocyte implantation (HD-ACI) in patients with bilateral knee chondral defects.
      Apart from the fact that having a single surgery recovery time is substantially reduced, as pointed out by Gordon et al.,
      • Gordon D
      • Crooks SA
      • Lewis TL
      • Ray R.
      Bilateral vs unilateral minimally invasive hallux valgus surgery: a propensity matched case-control study with 2 year clinical patient reported outcomes.
      performing one single procedure has a positive impact in the health system by reducing costs: it involves a single hospitalization and thus, total hospital stay is reduced; risks of anesthesia exposure are lower and rehabilitation time decreases, leading to earlier return of patients to their previous life status.
      This study represents a first approach to bilateral ankle chondral defects by simultaneous treatment with HD-ACI. In this case report we only describe the technique used in 2 patients and the results obtained after one-year follow-up. The number of patients with bilateral ankle or knee chondral defect with HD-ACI is very low, and thus, a study comparing treatment with one or two surgical procedures and with a longer follow-up period is now being planned, in order to define the advantages of having one or two surgeries.
      In conclusion, simultaneous treatment at the same surgical act with HD-ACI of both chondral defects of patients with bilateral cartilage defects in the ankle may be a good option. Patients undergoing this option have a satisfactory clinical outcome and a positive impact on their quality of life.

      Patient informed consent statement

      This work has been approved by the Educational and Research Committee of the Institution, and informed consent was obtained from the patients.

      Declaration of Competing Interests

      The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

      Acknowledgments

      We would like to thanks Mario Wensell for carefully revising the linguistics for this article.

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