Arthroscopic Non-Concentrated Autologous Iliac Bone Marrow Stimulation Shows Stable Medium-Term Clinical and Radiological Outcomes for Small Cystic Talar Osteochondral Lesions

Abstract

Objective

To evaluate radiological, short-term, and medium-term clinical outcomes of arthroscopic non-concentrated iliac bone marrow stimulation (BMS) for small talar cystic osteochondral lesions of the talus (OLTs).

Design

Forty-three cases underwent this modified BMS between 2014 and 2019 were evaluated. Clinical outcomes were assessed by the Foot and Ankle Ability Measure (FAAM) Activities of Daily Living (ADL) and Sports Subscales (SS). Regenerated tissue was evaluated with the Magnetic Resonance Observation of Cartilage Repair Tissue scales (MOCART-2.0). Subgroup analysis based on locations and concomitant anterior talofibular ligament (ATFL) injuries.

Results

The average diameter and depth of cysts were 6.97 ± 1.53 mm and 5.47 ± 1.10 mm, respectively. At a mean follow-up of 57.02 ± 19.61 months, FAAM-ADL and FAAM-SS improved significantly (45.65 ± 4.56 to 74.77 ± 8.03 and 12.63 ± 1.87 to 26.67 ± 3.41, respectively). From short-term to medium-term, FAAM-ADL revealed a minor decline (75.53 ± 7.76 vs. 74.77 ± 8.03, P = 0.421); FAAM-SS improved (25.37 ± 3.51 vs. 26.67 ± 3.41, P = 0.089). Medial lesions demonstrated favorable outcomes compared to lateral lesions [FAAM-ADL (77.04 ± 7.23 vs. 70.75 ± 8.10, P = 0.013), FAAM-SS (28.08 ± 2.40 vs. 24.19 ± 3.51, P < 0.001), and MOCART-2.0 (85.19 ± 11.27 vs. 71.88 ± 11.09, P < 0.001)]. Lateral lesions indicated higher rates of major hypertrophy (56.25% vs. 7.69%) and split-like defects (56.25% vs. 15.38%). The ATFL injuries did not significantly influence revision rates (15.8% vs. 4.2%, P = 0.439).

Conclusions

Arthroscopic non-concentrated iliac BMS demonstrated stable outcomes for small cystic OLTs. Lateral lesions were associated with inferior subjective scores and relatively higher rates of irregular fibrocartilage.

Keywords

cartilage arthroscopy talar osteochondral lesion bone marrow stimulation autologous iliac bone marrow

Introduction

Osteochondral lesions of the talus (OLTs) are relatively common lesions that affect the articular cartilage and subchondral bone after an ankle trauma. Bone marrow stimulation (BMS) procedures generally considered the first line of treatment for symptomatic OLTs smaller than 10 mm in diameter due to effectiveness, procedural simplicity, and relatively low complication rates.^1-3 In a recent literature, the success rate of BMS procedures for OLTs was 82% at a minimum follow-up of 10 years.⁴ Some scholars still hold different views on the medium- and long-term results of regular BMS procedures for OLTs due to the deterioration of the regenerated fibrocartilage.^5-8

There is notable concern on the applicability of standard arthroscopic BMS procedures for small cystic OLTs regarding their long-term efficacy.^3,9-12 Based on Ferkel et al.’s¹³ proposal, small cystic OLTs (defined at a depth ≤7 mm) can be treated effectively using regular BMS procedure without a bone graft. Some recent studies reported that small cystic OLTs (average depth ≤6 mm) may not influence the final results of arthroscopic BMS procedures.^14,15 The formation process of a “super clot” for fibrocartilage regeneration is dependent on the local blood supply and the available mesenchymal stem cells.^16,17 This unique anatomic characteristic of the subchondral vascularity of the talar dome might result in an “insufficient clot” in regular BMS procedures.¹⁸ Kim et al.¹⁹ highlighted that combining mesenchymal stem cells (MSCs) with a BMS procedure showed encouraging outcomes for small cystic OLTs. Various commercial devices for concentrated autologous bone marrow-derived cells also have emerged to enhance regular BMS effectiveness for OLTs repair.^20,21 The clinical evidence of adjuvant biologics with BMS procedures that can provide better outcomes of OLTs is still limited.²² Compared with concentrated bone marrow, the non-concentrated autologous BMS is simpler and more cost-effective with a lower risk of infection.^23,24 Furthermore, limited research focused on non-concentrated autologous iliac BMS for small cystic OLTs, leaving a gap with this issue.

The purpose of this study was to evaluate short-term and medium-term clinical outcomes and magnetic resonance image (MRI) findings of arthroscopic non-concentrated autologous iliac BMS for the treatment of small cystic OLTs (defined with an average diameter ≤10 mm, maximum depth ≤7 mm). Secondary aims included subgroup analysis of outcomes based on lesion locations and concomitant anterior talofibular ligament (ATFL) injuries. It was hypothesized that this modified BMS procedure would provide favorable outcomes for patients with small cystic OLTs.

Methods

This retrospective case series study was conducted in accordance with the Declaration of Helsinki and was approved by the Institutional Review Board of our hospital (No. [2023]083-01). The requirement for informed consent was waived by the ethics committee due to the retrospective nature of the study and the use of anonymized patient data.

From July 2014 to June 2019, patients with small cystic OLTs, which were treated by arthroscopic non-concentrated autologous iliac BMS in our hospital, were evaluated. On preoperative MRIs, the size of the cyst is not accurately measured due to the diffuse edema.¹⁷ The average diameter and maximum depth of the cyst were measured with Picture Arching and Communication Systems (PACS) by a senior radiologist on preoperative axial, coronal, and sagittal computed tomography (CT) images.^13,14 The medial and central lesions showed round cysts; however, the lateral lesions contained ellipsoid cysts. So, the average diameter of the cavity was utilized to measure and analyze rather than anteroposterior (AP) or mediolateral (ML) diameter due to some ellipsoid cysts.²⁵ The average diameter was calculated with the maximum length of the lesion on the sagittal and coronal plane ( Fig. 1 ). The inclusion criteria (1) aged from 18 to 55 years and (2) diagnosed with small cystic OLTs at the talar dome on preoperative MRI and CT. The included small cystic lesions were measured on CT images with an average diameter ≤10.1 mm and a maximum depth ≤7.1 mm (0.1 mm was added in the consideration of the measurement inaccuracies with the PACS systems);¹³ (3) non-operative treatments with symptoms for more than 3 months and no response; and (4) normal lower extremity alignment. Exclusion criteria were as follows: (1) kissing lesions or joint space narrowing were identified on preoperative radiographic images; (2) multiple cystic lesions; (3) severe medical diseases and chronic inflammatory systemic disorders; and (4) with additional osteotomy procedures.

Figure 1.

The measurement method of cyst size.

Surgical Procedures

The patient was placed in a supine position with a soft pad under the ipsilateral hip. The foot was aligned at the end of the operation table. The tourniquet could be applied to improve arthroscopic visualization. With posterior lesions, a non-invasive retractor was utilized. A sterile field was prepared for the ipsilateral lower limb and anterior iliac crest. The standard anteromedial and anterolateral portals were established using the nick and spread technique. If ATFL lesions were confirmed, the accessory anterolateral (acAL) portal was then established. A small-sized suture anchor (2.8 mm Titanium or 2.9 mm OSTEOPAPTOR AB, Smith & Nephew, USA) was implanted into the footprint of the ATFL. The ATFL remnant was then stitched using an arthroscopic repair procedure, which was introduced previously.^26,27 The knot was not tightened at this stage.

The cartilage surface was assessed using a probe. The damaged cartilage and subchondral bone plate were then gently debrided with a small curved curette (Fig. 2A, B). The solid sclerotic bone of the cyst was also carefully debrided. A stable margin of healthy cartilage is maintained. The cavity bottom was then penetrated with a 45° small-joint micro–fracture awl up to a depth of 3 mm with 3 mm intervals ( Fig. 2C ).

Figure 2.

Surgical procedures of arthroscopic non-concentrated iliac bone marrow stimulation. (A) The sclerotic subchondral bone could be broken down to gain access to the cyst. (B) The solid sclerotic bone of the cyst was carefully debrided with a small curved curette. (C) The cavity bottom was penetrated with a 45° small joint micro–fracture awl. (D) The appropriate size gelatin sponge was used to fill the cavity. (E) The non-concentrated autologous bone marrow was then injected into the cavity. (F) A “high-quality super clot” was constructed in the defect.

The 18G needle and syringe preloaded with 0.5 ml anticoagulant citrate dextrose solution were used to aspirate autologous bone marrow from the anterior iliac crest. The cavity of the lesion site was drained with a motorized shaver to create a “dry cavity” while irrigation was shut down. The appropriate size absorbable gelatin sponge (XIANG-EN Medical Co. Ltd., China) was then used to fill the cavity ( Fig. 2D ). In total, 2 ml non-concentrated autologous bone marrow was injected into the cavity (Fig. 2E, F). The knot of the stitched ATFL remnant suture was then tightened at this point in those individual cases with ATFL lesions. The incisions were closed with 3-0 Prolene sutures.

Postoperative Management

Twenty-four hours postoperative, continuous passive motion (CPM) machine was utilized for 4 to 6 hours a day in physical therapy. Crutches were utilized for 4 weeks to allow non-weightbearing exercise. After 4 weeks, 20 kg partial-weightbearing, walking with the use of air boots (The Rebound Air Walker, OSSUR Inc., Iceland) was encouraged. Rehabilitation exercises including strengthening of the lower extreme muscles and proprioceptive neuromuscular facilitation (PNF) were recommended for the following period. The patients could gradually resume low-impact activities after 3 months, including jogging, swimming, and cycling. However, returning to competitive sports is prohibited before 6 months postoperative.

Follow-up Assessment

Patients had a postoperative examination schedule at 3, 6, 12, and 24 months, then yearly. The postoperative 12 to 24 months was defined as short-term; postoperative 36 to 60 months was defined as medium-term.^17,28 The Foot and Ankle Ability Measure (FAAM) scales, including activities of daily living (ADL) and sports subscales (SS), were utilized to evaluate the preoperative situation and postoperative clinical outcomes.²⁹ Patients’ FAAM scores were recorded during out-patient follow-up visits before surgery and each year after the 12-month postoperative period by 2 senior clinicians. The quality of the regenerated tissue at the lesion site was assessed using the Magnetic Resonance Observation of Cartilage Repair Tissue scales (MOCART-2.0)³⁰ at the final follow-up. These measurements were confirmed by 2 senior clinicians and a radiologist. If inconsistencies occurred, another senior radiologist was consulted and the diagnosis was agreed upon by consensus. When possible, final postoperative CT was obtained to assess the subchondral bone regeneration. The subgroup analysis was explored based on different lesion locations and concomitant ATFL injuries. The surgical complications (superficial or deep infection, delayed incision healing, and nerve injuries) and revision surgeries were also recorded and assessed.

Statistical Analysis

All statistical analyses and data visualization were performed using Stata (18.0, Stata Corp LLC, College Station, TX, USA). Statistical significance difference was defined as P < 0.05. We assessed the normality of continuous baseline characteristics (e.g., age and body mass index [BMI]) using visual inspection of histograms. Normally distributed data were described as mean ± standard deviation. Non-normally distributed data were reported as median + interquartile range. For categorical variables, data were presented as number (n) and percentage (%). Given the case series study design, non-parametric tests were employed for all analyses. We conducted the Wilcoxon signed-rank test to compare preoperative and postoperative scores and to compare short-term vs. medium-term outcomes. We used the Mann-Whitney U-test to compare outcomes between subgroups (medial vs. lateral lesions; patients with vs. without ATFL lesions). P-values were reported for all statistical comparisons to indicate the significance of the findings.

Results

Patient Characteristics

We initially identified 51 patients with small-sized cystic OLTs, which were treated with this technique. Forty-three patients that met the inclusion criteria were finally included and assessed, with 8 patients being excluded that stopped their follow-up appointments after 12 months postoperative ( Fig. 3 ). The average follow-up time was 57.02 ± 19.61 months. The demographic characteristics of patients at the baseline are shown in Table 1 . More than half of patients (27, 62.8%) had a physically demanding job (athletes, soldiers). Twenty-six patients (60.5%) had medial lesions, 16 cases (37.2%) had lateral lesions, and only 1 (2.3%) had a central lesion. The mean diameter and depth of cysts were 6.97 ± 1.53 mm and 5.47 ± 1.10 mm, respectively. The majority of lesions were located in Zone 4 (48.8%) and Zone 6 (23.3%) according to the 9-zone grid system.³¹ Nineteen cases (44.2%) with chronic ATFL injuries underwent concurrent ligament repair surgery. We excluded the central lesion case from subgroup statistical analysis due to there being only 1 case.

Figure 3.

Flowchart of patients’ enrolling and grouping.

Table 1.

Demographic Characteristics of Participants at the Baseline.

Variables	Statistics (N = 43)
Age, years
Mean ± SD	32.84 ± 9.26
Cyst diameter, mm
Mean ± SD	6.97 ± 1.53
Cyst depth, mm
Mean ± SD	5.47 ± 1.10
Short-term follow-up time, mth
Mean ± SD	17.86 ± 5.10
Medium-term follow-up time, mth
Mean ± SD	57.02 ± 19.61
BMI, kg/m²
Mean ± SD	21.79 ± 2.67
Gender, n (%)
Male	31 (72.1)
Female	12 (27.9)
Injury side, n (%)
Left	17 (39.5)
Right	26 (60.5)
Occupation, n (%)
Soldier	19 (44.2)
Athlete	8 (18.6)
Worker	12 (27.9)
Student	4 (9.3)
Concomitant ATFL lesions, n (%)
Yes	19 (44.2)
No	24 (55.8)
OLT location, n (%)
Medial	26 (60.5)
Lateral	16 (37.2)
Central	1 (2.3)
Nine-zone grid, n (%)
Zone 4	21 (48.8)
Zone 6	10 (23.3)
Zone 3	6 (14.0)
Zone 1	3 (7.0)
Zone 7	2 (4.6)
Zone 5	1 (2.3)

Patient’s descriptive statistics in continuous variables were reported as mean ± standard deviation (SD); categorical variables were reported as number (n) and percentage (%).

BMI = body mass index; OLT = osteochondral lesion of talus; Mth = month.

Clinical Outcomes and Complications

The FAAM-ADL scores improved from 45.65 ± 4.56 at the baseline to 74.77 ± 8.03 at the final follow-up. Similarly, FAAM-SS scores showed an improvement from 12.63 ± 1.87 to 26.67 ± 3.41. The FAAM-ADL scores declined from 75.53 ± 7.76 to 74.77 ± 8.03 between short-term and medium-term follow-ups (P = 0.421). However, the FAAM-SS scores improved from short-term to medium-term follow-ups (25.37 ± 3.51 vs. 26.67 ± 3.41, P = 0.089). No superficial or deep infection, delayed incision healing, and nerve injuries were encountered. No recurrence of ankle instability was also observed in patients who underwent ATFL repair. The total proportion of OLT revision surgeries was 9.3% (4 cases), including second debridement (2 cases) and mosaicplasty (2 cases).

Details of Patients’ MOCART-2.0 Categories

Significant correlations were found between lesion locations and several MOCART-2.0 categories ( Table 2 and Figs. 4 and 5 ). Chi-square analysis revealed that medial and lateral lesions differed significantly in volume of cartilage defect filling (χ² = 16.66, P < 0.001), integration into adjacent cartilage (χ² = 7.74, P = 0.005), surface of the repair tissue (χ² = 8.40, P = 0.015), and structure of the repair tissue (χ² = 4.75, P = 0.029).

Table 2.

Individual MOCART-2.0 Categories of the Cases With Medial or Lateral Lesions.

Variables	Medial (n = 26)	Lateral (n = 16)	χ²	P
Volume of cartilage defect filling, n (%)			16.66	<0.001*
Complete filling	21 (80.8)	3 (18.7)
Major hypertrophy	2 (7.7)	9 (56.3)
50% to 74% filling of total defect volume	3 (11.5)	4 (25.0)
Integration into adjacent cartilage, n (%)			7.74	0.005*
Complete integration	22 (84.6)	7 (43.7)
Split-like defect at repair tissue and native cartilage interface ≤2 mm	4 (14.4)	9 (56.3)
Surface of the repair tissue, n (%)			8.40	0.015*
Surface intact	15 (57.7)	2 (12.5)
Surface irregular <50% of the repair tissue diameter	8 (30.8)	10 (62.5)
Surface irregular ≥50% of the repair tissue diameter	3 (11.5)	4 (25.0)
Structure of the repair tissue, n (%)			4.75	0.029*
Homogeneous	20 (76.9)	7 (43.7)
Inhomogeneous	6 (23.1)	9 (56.3)
Signal intensity of the repair tissue, n (%)			0.03	0.860
Normal	2 (7.7)	1 (6.3)
Minor abnormal (minor hyperintense or minor hypointense)	24 (92.3)	15 (93.7)
Bony defect or bony overgrowth, n (%)			0.03	0.860
Yes	2 (7.7)	1 (6.3)
No	24 (92.3)	15 (93.7)
Subchondral bone changes, n (%)			0.30	0.862
No	11 (42.3)	6 (37.5)
Minor edema	13 (50.0)	8 (50.0)
Severe edema	2 (7.7)	2 (12.5)

Categorical variables were reported as number (n) and percentage (%).

Significant difference, P < 0.05.

Figure 4.

Case 33, male, 28 years old, (A, B) a medial, round cystic OLT (arrow). (C, D) The filling of the inhomogeneous repair tissue (arrow) at 48 months postoperative. (E) The completely integrated repair tissue was observed at 73 months postoperative (arrow). (F) Significantly lower T2 values in the regenerated fibrocartilage (white arrow) are shown on the colored T2 map.

Figure 5.

Case 2, male, 27 years old, (A, B) a lateral, ellipsoid cystic OLT (arrow). (C, D) The filling of the inhomogeneous repair tissue (arrow) at 36 months postoperative. (E) The inhomogeneous repair tissue is observed at 65 months postoperative (arrow). (F) A white arrow marks the minor hypertrophy of the regenerated tissue on the colored T2 map. Higher T2 values are also visible at the interface between the regenerated tissue and native cartilage of the lateral talar facet.

In terms of volume of cartilage defect filling, medial lesions showed a higher rate of complete filling (80.77% vs. 18.75% in lateral lesions), while lateral lesions demonstrated a higher rate of major hypertrophy (56.25% vs. 7.69% in medial lesions). For integration into adjacent cartilage, medial lesions had better complete integration (84.62% vs. 43.75% in lateral lesions), whereas lateral lesions showed a higher rate of split-like defects at the repair tissue and native cartilage interface (56.25% vs. 15.38% in medial lesions).

Regarding the surface of the repair tissue, intact surface was more common in medial lesions (57.69% vs. 12.50% in lateral lesions), while irregular surface (both <50% and ≥50% of repair tissue diameter) was more frequent in lateral lesions (87.5% vs. 42.31% in medial lesions). For structure of the repair tissue, homogeneous structure was more prevalent in medial lesions (76.92% vs. 43.75% in lateral lesions), and inhomogeneous structure was more common in lateral lesions (56.25% vs. 23.08% in medial lesions).

No significant differences between medial and lateral lesions were found in signal intensity of the repair tissue (P = 0.860), bony defect or bony overgrowth (P = 0.860), and subchondral bone changes (P = 0.862).

Subgroup Analysis with Various Lesion Locations

When comparing final outcomes between medial (n = 26) and lateral (n = 16) lesions, we found differences in all measured parameters. Patients with medial lesions demonstrated relatively higher FAAM-ADL scores than those with lateral lesions (77.04 ± 7.23 vs. 70.75 ± 8.10, P < 0.001) ( Fig. 6A ). Both subgroups showed improvements from the baseline, but the medial lesion subgroup maintained higher scores at both short-term and medium-term evaluations. The pattern was similar for FAAM-SS scores, with medial lesions showing relatively superior outcomes compared to lateral lesions at the final follow-up (28.08 ± 2.40 vs. 24.19 ± 3.51, P < 0.001) ( Fig. 6B ). The medial lesions show higher MOCART-2.0 scores than lateral lesions (85.19 ± 11.27 vs. 71.88 ± 11.09, P < 0.001) ( Fig. 6C ). As depicted in Figure 2C , the medial lesion subgroup demonstrated not only higher scores but also a more favorable interquartile range, indicating more consistent repaired tissue quality. One outlier in the medial lesion subgroup (score of 50) was noted but did not substantially affect the overall statistical comparison.

Figure 6.

Compared outcomes between medial (n = 26) and lateral lesions (n = 16) demonstrating preoperative, short-term, and medium-term FAAM-ADL scores (A) preoperative, short-term, and medium-term FAAM-sports scores (B), and MOCART 2.0 scores at final follow-ups (medium-term) (C). The boxes represent the interquartile range with the horizontal line indicating the median, whiskers showing the range, and dots representing the outliers.

The FAAM-ADL scores in the medial lesion subgroup showed relative stability between short-term and medium-term evaluations. The lateral lesion subgroup displayed more variability in outcomes, particularly in the medium-term measurements. In the FAAM-SS subscale, the medial lesion subgroup demonstrated continued improvement from short-term to medium-term, while the lateral subgroup showed more variability. However, there is no significant difference in revision procedures (18.8% vs. 3.8%, P = 0.291).

Subgroup Analysis of Patients With and Without Anterior Talofibular Ligament Lesions

We also compared outcomes between patients with concomitant ATFL lesions (n = 19) and those without concomitant ATFL lesions (n = 24). For FAAM-ADL scores ( Fig. 7A ), both subgroups showed substantial improvement from preoperative to short-term and medium-term follow-ups. At the medium-term evaluations, the subgroup with ATFL lesions showed more variability, with a wider interquartile range compared to the subgroup without ATFL lesions. Nevertheless, mean values were not significantly different between both subgroups (74.00 ± 8.67 vs. 75.37 ± 7.63, P = 0.496). The FAAM-SS scores ( Fig. 7B ) followed a similar pattern, with no significant differences at the final follow-up between the subgroups (26.31 ± 3.99 vs. 26.96 ± 2.94, P = 0.701). The MOCART-2.0 scores at the final follow-up showed similar median values between the subgroups (81.32 ± 14.70 vs. 79.38 ± 11.16, P = 0.361) ( Fig. 7C ). There is no significant difference in the proportion of the revision procedures for OLTs between cases with or without ATFL lesions (15.8% vs. 4.2%, P = 0.439).

Figure 7.

Compared outcomes between cases with (n = 19) and without (n = 24) concomitant ATFL lesions showing preoperative, short-term, and medium-term FAAM-ADL scores (A), preoperative, short-term, and medium-term FAAM-Sports scores (B), and MOCART 2.0 scores at final follow-ups (medium-term) (C). The boxes represent the interquartile range with the horizontal line indicating the median, whiskers showing the range, and dots representing the outliers.

Discussion

The primary finding of this study is that arthroscopic non-concentrated autologous iliac BMS has shown stable medium-term clinical outcomes for small cystic OLTs (defined average diameter ≤10 mm, maximum depth ≤7 mm, previously defined at a depth ≤7 mm by Ferkel et al.¹³). The clinical outcomes did not deteriorate significantly with the passage of time, providing medium-term evidence for the durability of this modified approach. Recent literatures reported that OLTs with small cysts may not obviously influence the outcomes of arthroscopic BMS procedures.^14,15 According to the international consensus, however, cystic lesions are a potential variable influencing final outcomes of BMS.¹¹ Iliac bone marrow is the preferred bone marrow-derived mesenchymal stem cells (BM-MSCs) source for cartilage repair due to superior chondrogenic differentiation potential.^32,33 Combination of MSCs with BMS showed favorable results in older patients (>50 years), particularly when a subchondral cyst was present.¹⁹ Employing commercial devices to concentrate BM-MSCs was also suggested for OLTs repair.^20,21 In the present study, non-concentrated autologous iliac bone marrow with a gelatin sponge (as a scaffold) was implanted into the debrided cavity to simply construct a “high-quality super clot.” A high-quality super clot could regenerate high-quality fibrocartilage. Non-concentrated autologous BMS could be more cost-effective and has a lower risk of infection, compared with concentrated bone marrow.^23,24 We observed minimal changes in clinical outcome scores from short-term to medium-term follow-ups, with some patients showing continued improvement while others maintained stable scores. This stability of outcomes over time is encouraging and suggests that the initial regeneration achieved could be durable through medium-term. Appropriate regenerated tissue in most small cystic OLTs was observed on the final MRIs. Reassuringly, remolding of the subchondral bone plate in the previous cavity was also observed on the additional final CT scans in all 17 cases.

The second finding is that there is a correlation between lesion locations and radiological outcomes. On the final MRIs, higher incidences of major hypertrophy, split-like defects, irregular surfaces, and inhomogeneous of the regenerated tissue were observed in lateral lesions, compared with medial lesions. In the fundamental study about BMS, appropriate stress stimulation is vital for a “super clot” to differentiate into high-quality fibrocartilage.³⁴ Dynamic compression and flow-induced shear stress, generated from the pressure of the synovial fluid during joint movement, beneficially affects the chondrogenic differentiation of MSCs.³⁵ However, a previous cadaveric study demonstrated that more shear stress exists in the lateral dome of the talus due to the impacts between the fibula and lateral aspect of the talus during ankle movement.³⁶ A potential vulnerability to shear force at the regenerated tissue and native tissue interface was speculated to be a potential source of fibrocartilage degradation.³⁷ The special mechanical properties of the ankle joint might also be another reason for the unsatisfactory outcomes in BMS techniques. In the present study, the proportion of split-like defects at the regenerated tissue and native cartilage interface increased distinctly (56.25% vs. 15.38%) in the lateral lesions. Lateral lesions also present a relatively higher risk of revision procedures (18.8% vs. 3.8%, P = 0.291). Moreover, final FAAM-ADL, FAAM-SS scores, and MOCART-2.0 scores are higher in the medial lesions. More shear stress might be a negative effect on the regeneration process of fibrocartilage after BMS procedures. Managing the shear stress during the regeneration process of the repaired tissue can be a future study.

No noticeable correlation was documented between concomitant ATFL lesions and clinical outcomes in this study. Li et al.’s³⁸ study revealed that BMS has a limited effect for medial OLTs in unstable ankles, even after restoring ankle stability. In Lee et al.’s³⁹ research, OLTs with unstable ankles displayed higher risk of clinical failure (American Orthopaedic Foot and Ankle Society [AOFAS] score less than 80). Furthermore, the concurrent arthroscopic treatment of OLTs with ligament repair demonstrated no substantial negative effect on the overall outcomes, except for a potential risk of motion restriction.⁴⁰ In the present study, no significant differences were found in postoperative FAAM-ADL, FAAM-SS, and MOCART-2.0 scores between cases with or without ATFL lesions. Recurrence of ankle instability was also not observed. Although there is no significant difference in the proportion of the revision procedures for OLTs, cases without ATFL repaired procedures still exhibited a relatively lower risk (4.2% vs. 15.8%, P = 0.439). This observation highlights the importance of further research into optimizing cartilage regeneration in conjunction with ligament repair.

This study has some limitations. First, the limitation stems from the retrospective investigation design; it does not adhere to optimal study design practices that would include power calculations. A prospective study will be conducted in the future. Second, a comparison study with regular BMS techniques or concentrated autologous bone marrow will be conducted in the future. Third, the FAAM scores are not specifically designed for evaluating the OLTs, in order to overcome the shortcomings of this scoring system, the MOCART-2.0 scales were added for assessing the regenerated fibrocartilage. Fourth, the MOCART-2.0 scales are not validated for the ankle joint and cannot replace an accurate assessment of a second-look under arthroscopy. However, we cannot obtain second-look images from most asymptomatic postoperative patients except for revision surgeries. Fifth, only 17 patients underwent additional CT scans due to medical insurance policy limitations; thus, the evaluation of bone regeneration on CT images was not fully included. Finally, central lesion (only 1 case) was not included in the subgroup analysis. Despite this, the present study still offers valuable information about arthroscopic BMS procedures for small cystic OLTs.

In conclusion, arthroscopic non-concentrated autologous iliac BMS has shown stable medium-term outcomes for small cystic OLTs (average diameter ≤10 mm, maximum depth ≤7 mm on CT images). The clinical outcomes did not deteriorate significantly from short-term to medium-term follow-ups. Lateral lesions were associated with inferior subjective clinical scores and relatively higher rates of regenerated tissue irregularities. The present study did not include a comparison of non-concentrated autologous iliac BMS with regular BMS; so, the potential value of the iliac bone marrow is still limited. Further comparative studies need to be conducted.

Footnotes

Acknowledgements

We would like to express gratitude to John Valerius, an English native speaker, for taking the time to revise this paper. We thank Xinchen Wu, MD, and Jie Zhang, MD, for obtaining the follow-up data and Huibing Tan, a radiologist, for the imaging’s measurement and assessment. We also thank Liuyi Chen, a public health MD from the UQ Center for Clinical Research, The University of Queensland, for taking the time to revise the statistical analysis.

ORCID iD

Shijun Wei

Ethical Considerations

Ethics approval of this study was obtained from the Institutional Ethical Committee of General Hospital of Central Theater Command (IRB: [2023]083-01).

Author Contributions

Boyu Zheng: manuscript preparation and literature research.

Fei Yan: Data analysis and manuscript revision.

Yanjun Zhong: Data analysis and statistical analysis.

Shijun Wei: Designed study and manuscript revision.

Helin Wu: Follow-up data assessment.

Feng Xu: Manuscript review.

All authors read and approved the final manuscript.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

Choi

Lee

. Arthroscopic microfracture for osteochondral lesions of the talus: functional outcomes at a mean of 6.7 years in 165 consecutive ankles. Am J Sports Med. 2020;48(1):153-8. doi:10.1177/0363546519887957.

Powers

Dowd

Giza

. Surgical treatment for osteochondral lesions of the talus. Arthroscopy. 2021;37(12):3393-6. doi:10.1016/j.arthro.2021.10.002.

Krause

Anwander

. Osteochondral lesion of the talus: still a problem? EFORT Open Rev. 2022;7(6):337-43. doi:10.1530/EOR-22-0024.

Rikken

QGH

Aalders

Dahmen

Sierevelt

Stufkens

SAS

Kerkhoffs

GMMJ

. Ten-year survival rate of 82% in 262 cases of arthroscopic bone marrow stimulation for osteochondral lesions of the talus. J Bone Joint Surg Am. 2024;106(14):1268-76. doi:10.2106/JBJS.23.01186.

Park

Cho

Han

Lee

. Bone marrow stimulation for osteochondral lesions of the talus: are clinical outcomes maintained 10 years later. Am J Sports Med. 2021;49(5):1220-6. doi:10.1177/0363546521992471.

Ferkel

Zanotti

Komenda

Sgaglione

Cheng

Applegate

, et al Arthroscopic treatment of chronic osteochondral lesions of the talus: long-term results. Am J Sports Med. 2008;36(9):1750-62. doi:10.1177/0363546508316773.

Toale

Shimozono

Mulvin

Dahmen

Kerkhoffs

GMMJ

Kennedy

. Midterm outcomes of bone marrow stimulation for primary osteochondral lesions of the talus: a systematic review. Orthop J Sports Med. 2019;7(10):2325967119879127. doi:10.1177/2325967119879127.

Rikken

QGH

Dahmen

Stufkens

SAS

Kerkhoffs

GMMJ

. Satisfactory long-term clinical outcomes after bone marrow stimulation of osteochondral lesions of the talus. Knee Surg Sports Traumatol Arthrosc. 2021;29(11):3525-33. doi:10.1007/s00167-021-06630-8.

Savva

Jabur

Davies

Saxby

. Osteochondral lesions of the talus: results of repeat arthroscopic debridement. Foot Ankle Int. 2007;28(6):669-73. doi:10.3113/FAI.2007.0669.

10.

Vreeken

Dahmen

Stornebrink

Emanuel

Walinga

Stufkens

SAS

, et al Second-look arthroscopy shows inferior cartilage after bone marrow stimulation compared with other operative techniques for osteochondral lesions of the talus: a systematic review and meta-analysis. Cartilage. Epub 2024 Feb 7. doi:10.1177/19476035241227332.

11.

Hannon

Bayer

Murawski

Canata

Clanton

Haverkamp

, et al Debridement, curettage, and bone marrow stimulation: proceedings of the international consensus meeting on cartilage repair of the ankle. Foot Ankle Int. 2018;39(1 Suppl):16S-22S. doi:10.1177/1071100718779392.

12.

Hurley

Stewart

Kennedy

Strauss

Calder

Ramasamy

. Current management strategies for osteochondral lesions of the talus. Bone Joint J. 2021;103-B(2):207-12. doi:10.1302/0301-620X.103B2.BJJ-2020-1167.R1.

13.

Kerker

Ferkel

. Articular cartilage defects of the ankle. In: Ferkel

, editor. Foot and ankle arthroscopy. Philadelphia (PA): Wolters Kluwer; 2017. p. 183-226.

14.

Guo

Yan

Liu

Zeng

. Comparison of arthroscopic microfracture for osteochondral lesions of the talus with and without small and shallow subchondral cysts. Foot Ankle Int. 2024;45(4):383-92. doi:10.1177/10711007241227936.

15.

Pan

Yan

Zhuang

Chen

Guo

, et al Osteochondral lesions of the talus with small cysts may not affect the outcome of arthroscopic microfracture: a systematic review and meta-analysis. Foot Ankle Surg. 2025;31:384-91. doi:10.1016/j.fas.2025.01.004.

16.

Veronesi

Zielli

Brogini

Artioli

Arceri

Mazzotti

, et al Scaffolds for osteochondral lesions of the talus: systematic review and meta-analysis of the last ten years literature. Bioengineering (Basel). 2024;11(10):970. doi:10.3390/bioengineering11100970.

17.

Solomon

Williams Warren

. Marrow stimulation and microfracture for the repair of articular cartilage lesions. In: Williams

III RJ

, editor. Cartilage repair strategies. Totowa (NJ): Humana Press Inc; 2015. p. 69-84.

18.

Lomax

Miller

Fogg

Jane Madeley

Senthil Kumar

. Quantitative assessment of the subchondral vascularity of the talar dome: a cadaveric study. Foot Ankle Surg. 2014;20(1):57-60. doi:10.1016/j.fas.2013.10.005.

19.

Kim

Park

Kim

Koh

. Clinical outcomes of mesenchymal stem cell injection with arthroscopic treatment in older patients with osteochondral lesions of the talus. Am J Sports Med. 2013;41(5):1090-9. doi:10.1177/0363546513479018.

20.

Giannini

Buda

Vannini

Cavallo

Grigolo

. One-step bone marrow-derived cell transplantation in talar osteochondral lesions. Clin Orthop Relat Res. 2009;467(12):3307-20. doi:10.1007/s11999-009-0885-8.

21.

Giannini

Buda

Battaglia

Cavallo

Ruffilli

Ramponi

, et al One-step repair in talar osteochondral lesions: 4-year clinical results and T2-mapping capability in outcome prediction. Am J Sports Med. 2013;41(3):511-8. doi:10.1177/0363546512467622.

22.

Seow

Ubillus

Azam

Mercer

Yasui

Hui

, et al Limited evidence of adjuvant biologics with bone marrow stimulation for the treatment of osteochondral lesion of the talus: a systematic review. Knee Surg Sports Traumatol Arthrosc. 2022;30(12):4238-49. doi:10.1007/s00167-022-07130-z.

23.

Mavrogenis

Karampikas

Zikopoulos

Sioutis

Mastrokalos

Koulalis

, et al Orthobiologics: a review. Int Orthop. 2023;47(7):1645-62. doi:10.1007/s00264-023-05803-z.

24.

Gaul

Bugbee

Hoenecke

Jr D’Lima

. A review of commercially available point-of-care devices to concentrate bone marrow for the treatment of osteoarthritis and focal cartilage lesions. Cartilage. 2019;10(4):387-94. doi:10.1177/1947603518768080.

25.

Van Diepen

Smithuis

Hollander

Dahmen

Emanuel

Stufkens

SAS

, et al Reporting of morphology, location, and size in the treatment of osteochondral lesions of the talus in 11,785 patients: a systematic review and meta-analysis. Cartilage. Epub 2024 Feb 16. doi:10.1177/19476035241229026.

26.

Wei

Liu

Han

Cai

. Clinical outcomes of a modified all-inside arthroscopic repair of anterior talofibular ligament for chronic ankle instability: a preliminary report. Medicine (Baltimore). 2019;98(36):e16734. doi:10.1097/MD.0000000000016734.

27.

Zhi

Zhang

Wang

Zou

, et al Absorbable suture anchor and knotless anchor techniques produced similar outcomes in arthroscopic anterior talofibular ligament repair. Knee Surg Sports Traumatol Arthrosc. 2022;30(6):2158-65. doi:10.1007/s00167-021-06855-7.

28.

Ahmad

Hoos

Perka

Stöckle

Braun

Konrads

. Follow-up definitions in clinical orthopaedic research: a systematic review. Bone Jt Open. 2021;2(5):344-50. doi:10.1302/2633-1462.25.BJO-2021-0007.R1.

29.

Martin

Irrgang

Burdett

Conti

Van Swearingen

. Evidence of validity for the foot and ankle ability measure (FAAM). Foot Ankle Int. 2005;26(11):968-83. doi:10.1177/107110070502601113.

30.

Schreiner

Raudner

Marlovits

Bohndorf

Weber

Zalaudek

, et al The MOCART (Magnetic Resonance Observation of Cartilage Repair Tissue) 2.0 knee score and atlas. Cartilage. 2021;13(1 Suppl):571S-587S. doi:10.1177/1947603519865308.

31.

Raikin

Elias

Zoga

Morrison

Besser

Schweitzer

. Osteochondral lesions of the talus: localization and morphologic data from 424 patients using a novel anatomical grid scheme. Foot Ankle Int. 2007;28(2):154-61. doi:10.3113/FAI.2007.0154.

32.

Bernardo

Emons

Karperien

Nauta

Willemze

Roelofs

, et al Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources. Connect Tissue Res. 2007;48(3):132-40. doi:10.1080/03008200701228464.

33.

Scharstuhl

Schewe

Benz

Gaissmaier

Buhring

Stoop

. Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology. Stem Cells. 2007;25(12):3244-51. doi:10.1634/stemcells.2007-0300.

34.

Steadman

Rodkey

Rodrigo

. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res. 2001;(391 Suppl):S362-S369. doi:10.1097/00003086-200110001-00033.

35.

Zhang

Yao

. The role of mechanical regulation in cartilage tissue engineering. Curr Stem Cell Res Ther. 2021;16(8):939-48. doi:10.2174/1574888X16666210303151538.

36.

Athanasiou

Niederauer

Schenck

Jr.

Biomechanical topography of human ankle cartilage. Ann Biomed Eng. 1995;23(5):697-704. doi:10.1007/BF02584467.

37.

Shapiro

Koide

Glimcher

. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am. 1993;75(4):532-53. doi:10.2106/00004623-199304000-00009.

38.

Hua

Chen

. Treatment of talus osteochondral defects in chronic lateral unstable ankles: small-sized lateral chondral lesions had good clinical outcomes. Knee Surg Sports Traumatol Arthrosc. 2018;26(7):2116-22. doi:10.1007/s00167-017-4591-x.

39.

Lee

Kwon

Choi

Lee

. Comparison of outcomes for osteochondral lesions of the talus with and without chronic lateral ankle instability. Foot Ankle Int. 2015;36(9):1050-7. doi:10.1177/1071100715581477.

40.

Jiang

Jiao

Xie

Chen

Guo

, et al Concurrent arthroscopic osteochondral lesion treatment and lateral ankle ligament repair has no substantial effect on the outcome of chronic lateral ankle instability. Knee Surg Sports Traumatol Arthrosc. 2018;26(10):3129-34. doi:10.1007/s00167-017-4774-5.