Short-term radiological results after spheroid-based autologous chondrocyte implantation in the knee are independent of defect localisation

Abstract

BACKGROUND:

Lesions of articular cartilage represent a crucial risk factor for the early development of osteoarthritis. Autologous chondrocyte implantation (ACI) is a well-established procedure in therapy of those lesions in the knee. The aim of the presented study is to detect differences in short-term radiological outcome depending on defect localization (femoral condyle vs. retropatellar) after spheroid-based ACI.

OBJECTIVE:

This study aimed to demonstrate that radiological outcome after spheroid-based ACI in the knee is independent of defect localization.

METHODS:

MRI-scans after retropatellar ACI and ACI of the medial/lateral femoral condyle, with a preoperative Outerbridge grade of III or IV were evaluated regarding MOCART 2.0.

RESULTS:

The mean defect-size was 5.0 $\pm$ 1.8 cm ${}^{2}$ , with a minimum size of 2 cm ${}^{2}$ and a maximum size of 9 cm ${}^{2}$ . Scans were performed 7.7 months ( $\pm$ 3.1 months) postoperatively. The mean MOCART 2.0 score was 78.5 $\pm$ 15.6. No statistically significant influence neither of the localization ( $p=$ 0.159), the gender ( $p=$ 0.124) nor defect size ( $<$ 5 cm ${}^{2}$ vs. $\geqslant$ 5 cm ${}^{2}$ ; $p=$ 0.201) could be observed.

CONCLUSIONS:

The presented data demonstrate good to excellent radiological short-term results after spheroid-based ACI. Data indicates, that at least radiological results are independent of gender, defect-size and defect-localization.

Keywords

Knee cartilage autologous chondrocyte implantation spheroids osteoarthritis ACI

1. Introduction

Lesions of the articular cartilage represent a crucial risk factor for the early development of osteoarthritis, which could lead to complete destruction of the joint. Furthermore, osteoarthritis leads to pain and immobilization, and finally it represents a high burden for the health care systems.

Hyaline cartilage represents a unique structure, which is composed of water (70–80%) and extracellular matrix (ECM) with low cellularity and without any blood vessels or nerve fibres [1, 2]. This structure and its special biochemical composition enable hyaline cartilage to deform under pressure and remodels itself into its original form when pressure decreases [3]. However, hyaline cartilage nearly has no capacity to regenerate after trauma, which means that cartilage defects can lead to accelerated degradation of the joint, especially in younger people.

To prevent this and to postpone degenerative changes, different strategies are available for the treatment of cartilage lesions such as mosaic arthroplasty, microfracture, autologous matrix-induced chondrogenesis (AMIC) and autologous chondrocyte implantation (ACI). A relatively new technique represents the “minced cartilage” repair technique, a single-stage procedure, which uses minced cartilage from a less weight-bearing area of the knee. Massen et al. report satisfactory results after treatment of cartilage defects in the knee [4]. However long-term results and histological results are missing for this technique.

Matrix-based ACI (MACI) represents a third generation ACI. In contrast to first and second generation ACI, cultured cells are seeded on a scaffold, which gets implanted in the defect or come as spheroids. There is no need any more of covering the defect with f. e. periostal or collagen flaps [5, 6]. Moreover, spheroids do not require special fixation. Another advantage described, is that extracted cells keep their phenotype and do not dedifferenciate, like it is typical for chondrocytes in a foreign environment [5, 7]. Nevertheless, there is evidence, that MACI does not offer a significant superiority versus conventional ACI [8]. Bartlett et al. report about 42.9% hyaline cartilage in ACI treated defects, while MACI reached 36.4% here [9]. Taken these findings together, it can be concluded that that MACI simplifies the surgical intervention but does not deliver a significant better performance.

Various studies investigated the effectiveness of these strategies clinically, radiologically and histologically. The comparison of ACI with mosaic arthroplasty by Bentley et al. revealed excellent results in all cases [10]. Zeifang et al. compared ACI with MACI and reported no significant differences in these techniques by using the IKDC-score, Tegner-activity and the SF-36, but significant better results in the Lysholm-score for the ACI-P [8]. In 17 of the 21 patients, radiological MOCART score was performed, where ACI seemed to perform better than MACI again. Gooding et al. [11] could not detect significant differences between ACI covered with a periostal flap (ACI-P) and ACI covered with a collagen membrane (ACI-C) by performing histological safranin-O staining. A large histological evaluation of ACI was performed by McCarthy et al. Authors found good results for both techniques, with a slight superiority in the clinical outcome for ACI-C, even when the histological ICRS II score did not show a significant difference [12]. Compared to other techniques, a relatively small amount of literature deals with spheroid-based ACI.

Spheroid-based ACI showed superiority compared to microfracture in Activities of Daily Living at 24 months and Knee-related Quality of Life at 12 months [13], demonstrated excellent histological results [14] and proved safety and efficacy [15]. Niemeyer et al. examined the clinical outcome and success of ACI for cartilage defects of the patella and concluded that it leads to a high success rate with better results than the already excellent results in patients with the defects of the femoral condyle [16]. Mid-term results with a minimum follow-up of 4 years presented by Schlumberger et al. showed that ACI with in situ crosslinking matrix is a safe and reliable treatment for full-thickness cartilage defects of the knee [17].

Magnetic resonance imaging (MRI) is well established method in evaluation of chondro-regenerative therapies. Here, the MOCART-score has proven its worth and has lately been modified (“MOCART 2.0”) [18, 19].

In this study, we analysed 23 MRI-scans performed between 5 and 19 months postoperatively after spheroid-based ACI using the MOCART 2.0. Despite the fact, that load retropatellar as well as after-treatment after ACI is quite different to the femoral condyles, our hypothesis H0 was, that radiological results after spheroid-based ACI on the knee are independent of lesion localisation.

2. Methods

Twenty-three patients were treated with spheroid-based ACI (Spherox or Chondrospehere, Co.don, Teltow, Germany) due to focal chondral lesions retropatellar or of the medial femoral condyle, respectively the lateral femoral condyle in on case, with an Outerbridge grade of III or IV. ACI was performed as a two-stage procedure. In a first surgery, two cartilage-bone cylinders were harvested using a standardized cartilage biopsy tool with a diameter of 4 mm (Storz, Tuttlingen, Germany) from the intercondylar notch arthroscopically. After cell cultivation, the transplant comes in spheroid-form, small spheres, which contain of around 200.000 chondrocytes each. Implantation of delivered spheroids was performed via mini-arthrotomy and the use of a tourniquet with a pressure of 250 mmHg as a standard procedure following a period of approximately 8 weeks. Despite the fact, that implantation can be performed arthroscopically [20] when using the spheroids, we prefer a mini-open technique due to better transplant control in case of transplant-disclocation. Spheroids were applied after debridement of the cartilage defect to the subchondral bone trying to avoid bleeding for the subchondral bone. A special fixation of spheroids is not required. In case the defect was located retropatellar, up-standing of the patella was performed using a 2 mm k-wire as a joystick. Patients who underwent additional surgical procedures at the same time (f. e. MPFL-reconstruction, trochlea reconstruction) were excluded from the study. All patients included showed physiological leg axis, confirmed by anterior-posterior X-ray of the whole leg preoperatively. MRI scans of 23 knees after spheroid-based ACI were evaluated. Postoperative treatment followed our established standard and includes a magnetic resonance imaging (MRI)-scan between 6 and 12 months postoperatively.

MRI-imaging included the following sequences:

•
Proton-density weight spectral attenuated inversion recovery (PD SPAIR) were in all directions in space (axial, coronar, sagittal)
•
T1-weighted Turbo spin echo sequence (T1 TSE) in sagittal and coronar slides

All MRI scans were performed at a magnetic field strength of 3 Tesla (Philips Ingenia 3.0 T, Philips, Amsterdam, Netherlands) in our institute for diagnostically and interventional radiology. MRI-scans were evaluated according the MOCART 2.0 criteria published by Schreiner et al. (Table 1) [19]. Statistical analysis was performed using SPSS 26 (Armonk, New York, USA). Due to non-normally distributed variables, Mann-Whitney U test was used for statistical analysis. A $p$ -value less than 0.05 was regarded as statistically significant. A positive vote of the local ethical committee was given (approval number 20-1513).

Table 1
Items addressed by the MOCART 2.0 score. MOCART $=$ Magnetic Resonance Imaging of Cartilage Repair Tissue

Scoring

1 Volume fill of cartilage defect

1 Complete filling or minor hypertrophy 100–150% filling of defect volume 20

2 Major hypertrophy $>$ 150% or 75–99% defect filling 15

3 50–75% filling 10

4 25–49% filling 5

5 Up to 25% filling or complete delamination 0

2 Integration into adjacent cartilage

1 Complete integration 15

2 Split-like defect at repair tissue and native cartilage interface $<$ 2 mm 10

3 Defect at repair tissue and native cartilage interface $>$ 2 mm but $<$ 0% of repair tissue length 5

4 Defect at repair tissue and native cartilage interface $>$ 50% of repair tissue length 0

3 Surface of repair tissue

1 Intact 10

2 Irregular $<$ 50% of repair tissue diameter 5

3 Irregular $>$ 50% of repair tissue diameter 0

4 Structure of repair tissue

1 Homogeneous 10

2 Inhomogeneous 0

5 Signal intensity of repair tissue

1 Normal 15

2 Minor normal-minor hyperintense or minor hypointense 10

3 Severly abnormal-almost fluid like or close to subchondral plate signal 0

6 Bony defect/bony overgrowth

1 No defect, no overgrowth 10

2 Bony defect: depth $<$ thickness of adjacent cartilage or overgrowth $<$ 50% of adjacent cartilage 5

3 Bony defect: depth $>$ thickness of adjacent cartilage or overgrowth $>$ 50% of adjacent cartilage 0

7 Subchondral changes

1 No major subchondral changes 20

2 Minor edema-like marrow signal-maximum diameter $<$ 50% of repair tissue diameter 15

3 Severe edema-like marrow signal-maximum diameter $>$ 50% of repair tissue diameter 10

4 Subchondral cyst $>$ 5 mm in longest diameter or necrosis-like signal 0

Table 2
Descriptive patient data with mean values and standard deviations for MOCART 2.0 and its subitems of the 23 MRI-scans

Mean value Standard deviation (SD)

Patient Age (years) 33.91 12.965

Volume fill of cartilage defect 17.61 5.194

Integration into adjacent cartilage 13.48 3.515

Surface of the repair tissue 5.87 3.252

Structure of the repair tissue 7.83 4.217

Signal intensity of the repair tissue 9.78 3.529

Bony defect or bony overgrowth 8.48 2.794

Subchondral changes 15.43 2.982

MOCART 2.0 78.48 15.626

Difference Surgery $\diamondsuit$ MRI in months 7.65 3.084

Defect size (cm ${}^{2}$ ) 5.09 1.807

Figure 1.
Failure of ACI on the medial femoral condyle with poor defect filling and a MOCART 2.0 of 25 in a 53-year old female. MRI scans show a sagittal (left) and a coronary (right) slide.

Figure 2.
Satisfying results after spheroid-based ACI. First row: MRI-scan after ACI on the medial femoral condyle in the coronar (left) and sagittal (right) view. Second row: MRI-scan after ACI retropatellar in the axial (left) and sagittal (right) view. K-wire entrance in the patella is detectable in the sagittal view (down right).

3. Results

			Scoring
1	Volume fill of cartilage defect
	1	Complete filling or minor hypertrophy 100–150% filling of defect volume	20
	2	Major hypertrophy $>$ 150% or 75–99% defect filling	15
	3	50–75% filling	10
	4	25–49% filling	5
	5	Up to 25% filling or complete delamination	0
2	Integration into adjacent cartilage
	1	Complete integration	15
	2	Split-like defect at repair tissue and native cartilage interface $<$ 2 mm	10
	3	Defect at repair tissue and native cartilage interface $>$ 2 mm but $<$ 0% of repair tissue length	5
	4	Defect at repair tissue and native cartilage interface $>$ 50% of repair tissue length	0
3	Surface of repair tissue
	1	Intact	10
	2	Irregular $<$ 50% of repair tissue diameter	5
	3	Irregular $>$ 50% of repair tissue diameter	0
4	Structure of repair tissue
	1	Homogeneous	10
	2	Inhomogeneous	0
5	Signal intensity of repair tissue
	1	Normal	15
	2	Minor normal-minor hyperintense or minor hypointense	10
	3	Severly abnormal-almost fluid like or close to subchondral plate signal	0
6	Bony defect/bony overgrowth
	1	No defect, no overgrowth	10
	2	Bony defect: depth $<$ thickness of adjacent cartilage or overgrowth $<$ 50% of adjacent cartilage	5
	3	Bony defect: depth $>$ thickness of adjacent cartilage or overgrowth $>$ 50% of adjacent cartilage	0
7	Subchondral changes
	1	No major subchondral changes	20
	2	Minor edema-like marrow signal-maximum diameter $<$ 50% of repair tissue diameter	15
	3	Severe edema-like marrow signal-maximum diameter $>$ 50% of repair tissue diameter	10
	4	Subchondral cyst $>$ 5 mm in longest diameter or necrosis-like signal	0

	Mean value	Standard deviation (SD)
Patient Age (years)	33.91	12.965
Volume fill of cartilage defect	17.61	5.194
Integration into adjacent cartilage	13.48	3.515
Surface of the repair tissue	5.87	3.252
Structure of the repair tissue	7.83	4.217
Signal intensity of the repair tissue	9.78	3.529
Bony defect or bony overgrowth	8.48	2.794
Subchondral changes	15.43	2.982
MOCART 2.0	78.48	15.626
Difference Surgery $\diamondsuit$ MRI in months	7.65	3.084
Defect size (cm ${}^{2}$ )	5.09	1.807

Twenty-three knee MRI-scans of 14 males and 9 females with a mean age of 33.9 years ( $\pm$ 13 years) were evaluated. Defects were located on the medial femoral condyle ( $N=$ 13), the lateral femoral condyle ( $N=$ 1) or retropatellar ( $N=$ 9) and showed a mean size of 5.0 $\pm$ 1.8 cm ${}^{2}$ , with a minimum size of 2 cm ${}^{2}$ and a maximum size of 9 cm ${}^{2}$ . There was no statistically significant difference regarding the defect size between the two groups (femoral condyle vs. retropatellar, $p=$ 0.563). 10 patients showed a lesion-size of $>$ 5 cm ${}^{2}$ , 13 lesions were $\geqslant$ 5 cm ${}^{2}$ . Scans were performed 7.7 months ( $\pm$ 3.1 months) postoperatively. The mean MOCART 2.0 score was 78.5 $\pm$ 15.6 (Table 2). One treatment failure of spheroid-based ACI occurred on the medial femoral condyle (Fig. 1), while 15 patients showed a MOCART 2.0 of 80 points or higher (Fig. 2). Statistical analysis revealed no statistically significant difference regarding the values for MOCART 2.0 score between the regenerative tissue after spheroid-based ACI on the femoral condyle and spheroid-based ACI retropatellar ( $p=$ 0.159). Moreover there were no statistically significant differences regarding the sub-items of MOCART 2.0 volume fill of cartilage defect, integration into adjacent cartilage, surface of the repair tissue, structure of the repair tissue, signal intensity of the repair tissue, bony defect or bony overgrowth and subchondral changes (Table 3) between the two groups. Also, no statistically significant influence neither of the sex ( $p=$ 0.124) nor the defect size ( $<$ 5 cm ${}^{2}$ vs. $\geqslant$ 5 cm ${}^{2}$ ; $p=$ 0.201) could be observed.

4. Discussion

In this study, we performed retrospective evaluation of 23 MRI-scans after spheroid-based ACI on the knee. The technique demonstrated good radiological results (Fig. 2) with a mean MOCART 2.0 score of 78.5 ( $\pm$ 15.6) 7.7 months ( $\pm$ 3.1 months) postoperatively. To our knowledge, this is the first research-paper, which shows, that short-term radiological outcome after spheroid-based ACI is independent of defect localization (retropatellar vs. femoral condyle) and defect size ( $<$ 5 cm ${}^{2}$ vs. $\geqslant$ 5 cm ${}^{2}$ ). As a result, we accept our H0. Compared to other ACI-techniques, a relatively small amount of research deals with spheroid-based ACI. However several studies described good clinical results after spheroid-based ACI [13, 21] according established questionnaires (f. e. Knee injury and Osteoarthritis Outcome Score (KOOS), International Knee Documentation Committee (IKDC) subjective knee evaluation form) as well as satisfying radiological [13, 22] and even histological and immunhistological results [14]. Yoon et al. showed good clinical outcomes and survival rates in a minimum of a 10 year follow-up [23]. Despite the vast majority of ACIs are performed on the knee, satisfying results are also described for the shoulder [24].

Table 3
$P$ -values for defect localisation (femoral condyle vs retropatellar) regarding MOCART 2.0 and its sub-items. There was no statistically significant difference regarding MOCART 2.0 or any subitem between ACI on the femoral condyle and retropatellar

Item	$p$ -value (femoral condyle vs retropatellar)
Volume fill of cartilage defect	0.277
Integration into adjacent cartilage	1.0
Surface of the repair tissue	0.336
Structure of the repair tissue	0.477
Signal intensity of the repair tissue	0.369
Bony defect or bony overgrowth	0.439
Subchondral changes	0.643
MOCART 2.0	0.159

MRI scans are the gold standard of non-invasive diagnostic for evaluate articular cartilage and articular cartilage repair tissue. In 2004, Marlovits et al. defined criteria for the Magnetic Resonance Observation of Cartilage Repair Tissue (MOCART)-score [25], which is established as standard in the evaluation of cartilage-repair procedures and allows an objective and standardized rating of the regenerated tissue. This score was further developed by Schreiner et al. with the introduction of MOCART 2.0 [19]. Authors argue, that MRI-imaging made distinct progress since introduction of MOCART, which made changes of the score necessary. Because of this, we decided to use MOCART 2.0. This fact may slightly limit the comparability with other studies, which used just MOCART.

Good radiological results for ACI were published by several authors [26, 27]. McCarthy et al. reported a mean MOCART of 70 12 months postoperatively for ACI with periostal flap (ACI-P) as well as for ACI with collagen membrane (ACI-C) and conclude, that MRI 12 months postoperatively can predict long-term results [26]. Beside good clinical and radiological results, Barie et al. reported revision-rates of ACI-P and MACI of around 30% in their long-term mean follow-up [27].

In our study, MOCART 2.0 results were not affected by defect size nor defect localization (medial femoral condyle and retropatellar). However, a higher patient-age as well as lesion $>$ 4.5 cm ${}^{2}$ were identified as risk-factors for a higher revision- and failure-rate in the review by Pareek et al., with revision-rates up to 50%. Some of these revisions were caused by graft hypertrophy and lysis of adhesions, but authors report a significant percentage of revision surgeries were caused by reasons, which represented a graft failure or a progression of osteoarthritis over time [28]. We want to admit, that in our opinion, a progress of osteoarthritis after 10 or more years does not necessarily represent a failure of ACI. The oldest patient included in this study was 54 years at time of surgery. Even when this patient would show up with a progress of osteoarthritis 10 years after ACI, we think it is hard to define this as a failure of the procedure. A high-grade osteoarthritis can occur in patients over 60 years on a regular basis without anamnestically existing chondral lesions.

Some limitations of the study have to be mentioned. The study presented only focused on radiological outcome of spheroid-based ACI and MRI-scans were performed relatively early postoperatively, which is why it’s expressiveness regarding clinical and long-term results is highly limited for sure, even authors predict good clinical long-term results, in case of good MRI results one year after surgery [26]. Our results showed that the cartilage recovery in a short-term follow-up is good to excellent, so there would maybe just a little benefit of a longer follow up. Patients want to know what’s going on in a short term and how it looks like within a half- or year after surgery. Moreover, even we could show good and in some cases excellent radiological results, we do not have tissue samples to collect histopathological data. Good histological and immunhistological results were described for this technique, but in a relatively small number of specimen [14]. It is challenging to obtain the specimen for histopathological evaluation, due to limited indications for re-arthroscopy and tissue-sampling. Nevertheless, histology is commonly considered the gold-standard for the evaluation of tissue-quality.

5. Conclusion

Footnotes

Conflict of interest

The authors declare that there is no conflict of interest.

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Short-term radiological results after spheroid-based autologous chondrocyte implantation in the knee are independent of defect localisation

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Methods

4. Discussion

Table 3 P -values for defect localisation (femoral condyle vs retropatellar) regarding MOCART 2.0 and its sub-items. There was no statistically significant difference regarding MOCART 2.0 or any subitem between ACI on the femoral condyle and retropatellar

Footnotes

Conflict of interest

References

Table 3
$P$ -values for defect localisation (femoral condyle vs retropatellar) regarding MOCART 2.0 and its sub-items. There was no statistically significant difference regarding MOCART 2.0 or any subitem between ACI on the femoral condyle and retropatellar