ISSN: 2329-910X
Clinical Research on Foot & Ankle
Make the best use of Scientific Research and information from our 700+ peer reviewed, Open Access Journals that operates with the help of 50,000+ Editorial Board Members and esteemed reviewers and 1000+ Scientific associations in Medical, Clinical, Pharmaceutical, Engineering, Technology and Management Fields.
Meet Inspiring Speakers and Experts at our 3000+ Global Conferenceseries Events with over 600+ Conferences, 1200+ Symposiums and 1200+ Workshops on Medical, Pharma, Engineering, Science, Technology and Business
Research Article Open Access
Macroscopic ICRS Poorly Correlates with O Driscoll Histological Cartilage Repair Assessment in a Goat Model
| Kok AC1*, van Bergen CJA1, Tuijthof GJM1,2, Klinkenbijl MN1, van Noorden CJF3, van Dijk CN1 and Kerkhoffs GMMJ1 | |
| 1Department of Orthopedic Surgery, Orthopedic Research Center Amsterdam, Academic Medical Center Amsterdam, the Netherlands | |
| 2BioMechanical Engineering, Faculty of Mechanical, Maritime and Materials Engineering, Delft University of Technology, the Netherlands | |
| 3Department of Cell Biology and Histology, Academic Medical Center Amsterdam, University of Amsterdam, the Netherlands | |
| Corresponding Author : | Kok AC Orthopedic Research Center Amsterdam Academic Medical Center, Amsterdam, The Netherlands Tel: +31071 5277057 E-mail: a.kok@amc.uva.nl |
| Received: June 19, 2015 Accepted: September 23, 2015 Published: September 26, 2015 | |
| Citation: Kok AC, van Bergen CJA, Tuijthof GJM, Klinkenbijl MN, van Noorden CJF, et al. (2015) Macroscopic ICRS Poorly Correlates with O’Driscoll Histological Cartilage Repair Assessment in a Goat Model. Clin Res Foot Ankle 3:173. doi:10.4172/2329-910X.1000173 | |
| Copyright: © 2015 Kok AC, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. | |
| Related article at Pubmed, Scholar Google | |
Visit for more related articles at Clinical Research on Foot & Ankle
Abstract
Background: The purpose of this research was to evaluate whether the macroscopic assessment of repair cartilage quality of talar osteochondral defects in a goat model using the ICRS score is in correspondence with histological assessment using the O’Driscoll histology score.
Methods: 32 caprine samples with six mm osteochondral defects treated with microfracture were analyzed six months postoperatively using high-resolution digital images. Two observers independently scored the defects using the ICRS (0-12 points). Histological analysis was performed by one expert histologist using the O’Driscoll Score (0-24 points) on 5 μm slices stained with Masson Goldner and Safranin O. Total ICRS and O’Driscoll scores as well as sub items were compared using a Spearman correlation coefficient (p<0.05).
Results: The median ICRS for Observer 1 and 2 were 6.5 (range: 4-11) and 6.5 (range: 3-11). The median O’Driscoll score was 11.5 (range: 3-20). The correlation of the total ICRS scores and the O’Driscoll score was not significant, nor was the correlation of sub items (p>0.05).
Conclusion: This animal study suggests that isolated macroscopic ICRS assessment of cartilage repair tissue does not correlate well with histological assessment. Possible explanations may be limitations of surface assessment compared to analysis deeper into the tissue and the necessity of more elaborate macroscopic assessment including hypertrophy, colour, lesion size, location and degenerative status of the joint. Techniques that are more accurate, precise and reliable, such as histology, dGEMERIC and T2 mapping MRI, contrast enhanced CT or optical coherence tomography (OCT), should be considered as alternatives or at least as complimentary methods.
Abstract
Background: The purpose of this research was to evaluate whether the macroscopic assessment of repair cartilage quality of talar osteochondral defects in a goat model using the ICRS score is in correspondence with histological assessment using the O’Driscoll histology score.
Methods: 32 caprine samples with six mm osteochondral defects treated with microfracture were analyzed six months postoperatively using high-resolution digital images. Two observers independently scored the defects using the ICRS (0-12 points). Histological analysis was performed by one expert histologist using the O’Driscoll Score (0-24 points) on 5 µm slices stained with Masson Goldner and Safranin O. Total ICRS and O’Driscoll scores as well as sub items were compared using a Spearman correlation coefficient (p<0.05).
Results: The median ICRS for Observer 1 and 2 were 6.5 (range: 4-11) and 6.5 (range: 3-11). The median O’Driscoll score was 11.5 (range: 3-20). The correlation of the total ICRS scores and the O’Driscoll score was not significant, nor was the correlation of sub items (p>0.05).
Conclusion: This animal study suggests that isolated macroscopic ICRS assessment of cartilage repair tissue does not correlate well with histological assessment. Possible explanations may be limitations of surface assessment compared to analysis deeper into the tissue and the necessity of more elaborate macroscopic assessment including hypertrophy, colour, lesion size, location and degenerative status of the joint. Techniques that are more accurate, precise and reliable, such as histology, dGEMERIC and T2 mapping MRI, contrast enhanced CT or optical coherence tomography (OCT), should be considered as alternatives or at least as complimentary methods.
Methods: 32 caprine samples with six mm osteochondral defects treated with microfracture were analyzed six months postoperatively using high-resolution digital images. Two observers independently scored the defects using the ICRS (0-12 points). Histological analysis was performed by one expert histologist using the O’Driscoll Score (0-24 points) on 5 µm slices stained with Masson Goldner and Safranin O. Total ICRS and O’Driscoll scores as well as sub items were compared using a Spearman correlation coefficient (p<0.05).
Results: The median ICRS for Observer 1 and 2 were 6.5 (range: 4-11) and 6.5 (range: 3-11). The median O’Driscoll score was 11.5 (range: 3-20). The correlation of the total ICRS scores and the O’Driscoll score was not significant, nor was the correlation of sub items (p>0.05).
Conclusion: This animal study suggests that isolated macroscopic ICRS assessment of cartilage repair tissue does not correlate well with histological assessment. Possible explanations may be limitations of surface assessment compared to analysis deeper into the tissue and the necessity of more elaborate macroscopic assessment including hypertrophy, colour, lesion size, location and degenerative status of the joint. Techniques that are more accurate, precise and reliable, such as histology, dGEMERIC and T2 mapping MRI, contrast enhanced CT or optical coherence tomography (OCT), should be considered as alternatives or at least as complimentary methods.
Keywords
Osteochondral defects; Talus; Goat model; ICRS cartilage repair assessment system; O’Driscoll histological assessment; Correlation
Introduction
Histological evaluation of cartilage repair tissue of after treatment of osteochondral defects is a longstanding and proven method for quality assessment with both qualitative and quantitative parameters [1]. Experimental animal studies often use histological analysis of the repair tissue after sacrifice of the animals [1-9]. In the case of clinical studies, a biopsy can be taken for histology [10-12]. Even though considered to be the gold standard, biopsies are usually not performed in a clinical setting because it destroys part of the repair tissue. In addition, the histological processing and subsequent analyses take time. This makes surgical intervention in 1 session with the assessment of the quality of repair based on the biopsy results not possible, necessitating a two-step procedure. Moreover, biopsies can only show the characteristics of that particular part of the lesion of which the biopsy was taken. Locational differences within the repair area are not detected. Furthermore, the quality of biopsy and the moment in follow-up of the acquisition affect the quality and result of the biopsy [13]. Therefore, histology of in vivo repaired tissue is generally restricted to a research setting, while in clinical practice, cartilage quality is assessed through imaging and intraoperative macroscopic evaluation by the surgeon [14].
Macroscopic assessment of the repair tissue during (second look) arthroscopy is used to assess the degree of defect fill, the aspect of repair tissue as well as its integration with adjacent cartilage after treatment [15]. It has shown to be associated with the clinical failure rate [16]. There are 2 validated grading systems in the literature that assess repair tissue quality during arthroscopy or open surgery, the Oswestry Arthroscopy Score (OAS) [17] and the International Cartilage Repair Society Cartilage Repair Assessment System (ICRS) [18]. Main components of both scores are the nature of the tissue (macroscopic appearance of the cartilage surface) and whether the repair tissue is satisfactory (the extent to which the original defect is filled with repair tissue and the integration of the repair tissue into the border zone). Both scores are used in the evaluation of human as well as animal repair tissue [5,19,20]. Other studies have reported satisfactory interobserver reliability and repeatability for both the ICRS and the OAS arthroscopic score with an ICC>0.7 and good correlation (Pearson’s correlation coefficient, r=0.88; P<0.001). Cronbach’s alpha was slightly better for the ICRS: 0.91 vs. 0.82 for the OAS [17,21].
There is no data that compares the macroscopic scores and findings from the histological quality assessment scores. Therefore, it is unknown to which extent these macroscopic scores correlate with the histological reference standard. A good correlation would strengthen diagnosis and evaluation based on arthroscopic assessment instead of histology, whereas a poor correlation would indicate that the score is insufficient for objective cartilage repair tissue assessment. The aim of this study was to evaluate the correlation of the macroscopic ICRS score to a histological score of repaired cartilage. The hypothesis was that the ICRS corresponds moderately with histological analysis, because the ICRS evaluates the surface of osteochondral lesions whereas histology also assesses deeper tissue layers.
Macroscopic assessment of the repair tissue during (second look) arthroscopy is used to assess the degree of defect fill, the aspect of repair tissue as well as its integration with adjacent cartilage after treatment [15]. It has shown to be associated with the clinical failure rate [16]. There are 2 validated grading systems in the literature that assess repair tissue quality during arthroscopy or open surgery, the Oswestry Arthroscopy Score (OAS) [17] and the International Cartilage Repair Society Cartilage Repair Assessment System (ICRS) [18]. Main components of both scores are the nature of the tissue (macroscopic appearance of the cartilage surface) and whether the repair tissue is satisfactory (the extent to which the original defect is filled with repair tissue and the integration of the repair tissue into the border zone). Both scores are used in the evaluation of human as well as animal repair tissue [5,19,20]. Other studies have reported satisfactory interobserver reliability and repeatability for both the ICRS and the OAS arthroscopic score with an ICC>0.7 and good correlation (Pearson’s correlation coefficient, r=0.88; P<0.001). Cronbach’s alpha was slightly better for the ICRS: 0.91 vs. 0.82 for the OAS [17,21].
There is no data that compares the macroscopic scores and findings from the histological quality assessment scores. Therefore, it is unknown to which extent these macroscopic scores correlate with the histological reference standard. A good correlation would strengthen diagnosis and evaluation based on arthroscopic assessment instead of histology, whereas a poor correlation would indicate that the score is insufficient for objective cartilage repair tissue assessment. The aim of this study was to evaluate the correlation of the macroscopic ICRS score to a histological score of repaired cartilage. The hypothesis was that the ICRS corresponds moderately with histological analysis, because the ICRS evaluates the surface of osteochondral lesions whereas histology also assesses deeper tissue layers.
Materials and Methods
Materials: 32 caprine samples of treated osteochondral defects treated were analysed 6 months postoperatively. The samples were retrieved from a study investigating the healing response of artificially created talar osteochondral defects of 16 goats treated with microfracture [22]. The study protocol was approved by the local Animal Welfare Committee (protocol number ORCA102287). A 6 mm diameter osteochondral defect was drilled in the tali of both hind legs using a posterolateral surgical approach. In the same surgical session, the goats received microfracture treatment using microfracture awls. The animals were allowed to directly bear weight postoperatively. The goats were sacrificed after a follow-up of 24 weeks, after which the tali were extracted and photographed in multiple directions using a high-resolution digital camera (Panasonic Lumix, Kadoma, Japan).
The tali were cut into 20 mm × 20 mm blocks around the defect over the entire depth of the talus [22]. The samples were embedded in Methylmetacrylate and 5 µm were cut at approximately a quarter and at the centre of each defect. Haematoxylin and Eosin (general staining), Safranin-O (GAG content) and Masson Goldner (Collagen) staining were performed multiple section for each location. Representative slices of both locations were selected for cartilage quality assessment.
Histologic scoring: Thirty histological sections were available per sample. All were scanned for quality of processing and staining. Selected histological sections were scored by 1 expert histologist (RvN) using the O’Driscoll histology score [23]. A recent review provides an overview of the existing histological scoring systems [9]. Both the O'Driscoll score [23] and the Pineda score [24] met our requirements of applicability for the assessment of cartilage repair and present available validation for animal studies [25]. The O’Driscoll score was used because of its extensiveness. The score by O’Driscoll contains 4 main categories and sub items, which gives a total score of a maximum of 24 points [23].
The tali were cut into 20 mm × 20 mm blocks around the defect over the entire depth of the talus [22]. The samples were embedded in Methylmetacrylate and 5 µm were cut at approximately a quarter and at the centre of each defect. Haematoxylin and Eosin (general staining), Safranin-O (GAG content) and Masson Goldner (Collagen) staining were performed multiple section for each location. Representative slices of both locations were selected for cartilage quality assessment.
Histologic scoring: Thirty histological sections were available per sample. All were scanned for quality of processing and staining. Selected histological sections were scored by 1 expert histologist (RvN) using the O’Driscoll histology score [23]. A recent review provides an overview of the existing histological scoring systems [9]. Both the O'Driscoll score [23] and the Pineda score [24] met our requirements of applicability for the assessment of cartilage repair and present available validation for animal studies [25]. The O’Driscoll score was used because of its extensiveness. The score by O’Driscoll contains 4 main categories and sub items, which gives a total score of a maximum of 24 points [23].
Statistical analysis
To test our hypothesis, the validity of the ICRS was determined by calculating the interobserver variability and the correlation between the O’Driscoll score and the ICRS. A sample size of 32 had 80% power to detect a minimum level of correlation of 0.4 (moderate correlation based on the definition of Landis and Koch [26]) with a 0.05 two-sided significance. A correlation above 0.4 was considered to be possible significance, since both Landis c.s. and Fleiss c.s. define a correlation below 0.4 as only poor to fair [26,27]. For the ICRS to be a reliable tool for cartilage repair assessment a less than moderate correlation coefficient is not desired. Due to skewed distributions and outliers, non-parametric Spearman’s correlation coefficients were calculated between the total O’Driscoll and ICRS scores, as well as between specific subsets. The subsets were chosen selected on the basis of the related themes of the scored items: Macroscopic appearance (ICRS) and Surface regularity (O’Driscoll score); and Integration to border zone (IRCS) and Bonding to the adjacent cartilage (O’Driscoll score). A p<0.05 was considered significant.
Results
ICRS: The median ICRS score was 6.5 (range 4-11) for Observer 1 and 6.5 (range (3-11) for Observer 2 (Table 1). The defects were classified mainly as a grade II (nearly normal, n=10 and n=15 for Observer 1 and 2, respectively), or a grade III (abnormal, n=22 and n=16 for Observer 1 and 2 respectively). Only Observer 2 classified one defect as grave IV (severely abnormal). The inter-observer agreement was 50% with a к of 0.4 (p<0.001) for the total ICRS score. The agreement for the sub items was higher.
Histology: The median O’Driscoll score of the samples was 11.5 (range 3-20, Table 2). All defects were predominantly filled with fibrous tissue, with diminished Safranin O staining and with large collagen structures visible using polarized light microscopy. The variety in surface appearance and structural integrity was substantial (Table 2 and Figure 1).
Correlations: The Spearman’s rank correlation coefficient of the average total ICRS score for either observers or the O’Driscoll score was not significant (Observer 1: ρ=-0.004, p=0.98, 95% CI=0.40-0.37, Observer 2: ρ=-0.132, p=0.47, 95% CI=0.53-0.29, Figure 2). Likewise, the correlations were not statistically significant for the specific subsets of macroscopic appearance (ICRS) and surface regularity (O’Driscoll score) or for the subset integration to border zone (IRCS) and bonding to the adjacent cartilage (O’Driscoll score) (Table 3).
Histology: The median O’Driscoll score of the samples was 11.5 (range 3-20, Table 2). All defects were predominantly filled with fibrous tissue, with diminished Safranin O staining and with large collagen structures visible using polarized light microscopy. The variety in surface appearance and structural integrity was substantial (Table 2 and Figure 1).
Correlations: The Spearman’s rank correlation coefficient of the average total ICRS score for either observers or the O’Driscoll score was not significant (Observer 1: ρ=-0.004, p=0.98, 95% CI=0.40-0.37, Observer 2: ρ=-0.132, p=0.47, 95% CI=0.53-0.29, Figure 2). Likewise, the correlations were not statistically significant for the specific subsets of macroscopic appearance (ICRS) and surface regularity (O’Driscoll score) or for the subset integration to border zone (IRCS) and bonding to the adjacent cartilage (O’Driscoll score) (Table 3).
Discussion
The aim of this study was to assess the correlation between the macroscopic cartilage repair tissue assessment using the ICRS score and the histological assessment using the O’Driscoll score after microfracture treatment of talar osteochondral defects in a goat model. Our hypothesis was that the scores would correlate moderately, however, no significant correlation was found between both scores.
Strengths of this study are the use of a validated goat model, 2 surgeons with extensive clinical experience with arthroscopic cartilage repair, as well as an expert histologist familiar with cartilage repair histology. However, the number of samples was limited and the average quality of the fibrous repair tissue did not cover the full range of the O’Driscoll score (range 3-20 vs. 0-24). These 2 factors may at least in part have contributed the absence of a correlation. Also, the macroscopic scoring was not performed in vivo, but by means of post mortem photographs. Although this is a method that is frequently used in a variety of studies for macroscopic scoring of cartilage [21,28,29], it does not allow the freedom of assessment from all angles as in vivo arthroscopy does. Lastly, the study was designed to detect a correlation larger than 0.4, because a correlation smaller than this was considered to be clinically irrelevant. A more subtle correlation could be present between the scores or sub items.
Apart from limitations in the study design, several characteristics of the ICRS score may also have affected the lack of correlation. Firstly, only extreme structural disorganizations such as large clefts can be registered by the macroscopic score (Figure 1A), whereas subtle structural differences, such as smaller fissures or cysts hidden from the macroscopic surface (Figure 1B), are not detected. This leads to overestimation of the quality of repair tissue by macroscopic assessment compared to histological measures (Figure 2).
Secondly, the lack of correlation could be explained by the introduction of individual judgement in the ICRS score, because both the degree of defect fill and measurement of the demarcating border require the observer to determine quantitative values based on individual estimations. It could be possible that repeated individual scoring results in a different score. Previous articles did not specify the degree of experience with the ICRS scoring of the observers, but one article did show a significant increase in inter observer agreement after 2 months training [30]. Whether this also influences the correlation to histology remains to be investigated.
Thirdly, the ICRS does not allow the observer to report graft hypertrophy, nor does it include the colour aspect of the defect. Both items have been discussed in literature to be of relative importance and are included in the Oswestry Arthroscopy scale. However, we were not able to detect a colour difference as used by the OAS (pearly hyaline-like, white fibrous tissue, yellow bone) between our samples with a good or a poor O’Driscoll score, since all were more or less white fibrous tissue.
Moreover, the O’Driscoll score assesses the borders in one plane and is location dependent, while the ICRS score takes the entire defect rim into consideration and judges the percentage of the rim that is attached. This explanation is supported by the fact that no correlation was found between the sub item scores for the integration of the repair tissue into the border zone.
The results indicate that despite the satisfactory inter observer reliability found previously, ICRS scoring may not be an accurate manner to determine cartilage or repair quality during arthroscopy. Arthroscopy also allows for assessment of multiple domains such as the size of the lesion and the general state of degeneration of the joint. Since these are all features that influence the healing or possible deterioration of cartilage defects, these items could be added in the score. to make the ICRS scoring more accurate [27,31-33].
For research purposes, alternatives of histology that are more accurate, precise and reliable should be considered, such as dGEMERIC and T2 mapping MRI, contrast enhanced CT or optical coherence tomography (OCT) [34]. These techniques are also applied more and more in clinical practice and according to the increasing amount of literature of these advanced techniques image parameters correlate highly with cartilage quality [35-38].
In conclusion, this animal study suggests that isolated macroscopic assessment of the quality of cartilage repair tissue of talar osteochondral defects treated with micro fracture using the ICRS score has a poor correlation with histological analysis. Possible explanations may be found in the limitations of surface assessment compared to analysis deeper into the tissue and the necessity of more elaborate macroscopic assessment including hypertrophy, colour, lesion size, location and degenerative status of the joint.
Strengths of this study are the use of a validated goat model, 2 surgeons with extensive clinical experience with arthroscopic cartilage repair, as well as an expert histologist familiar with cartilage repair histology. However, the number of samples was limited and the average quality of the fibrous repair tissue did not cover the full range of the O’Driscoll score (range 3-20 vs. 0-24). These 2 factors may at least in part have contributed the absence of a correlation. Also, the macroscopic scoring was not performed in vivo, but by means of post mortem photographs. Although this is a method that is frequently used in a variety of studies for macroscopic scoring of cartilage [21,28,29], it does not allow the freedom of assessment from all angles as in vivo arthroscopy does. Lastly, the study was designed to detect a correlation larger than 0.4, because a correlation smaller than this was considered to be clinically irrelevant. A more subtle correlation could be present between the scores or sub items.
Apart from limitations in the study design, several characteristics of the ICRS score may also have affected the lack of correlation. Firstly, only extreme structural disorganizations such as large clefts can be registered by the macroscopic score (Figure 1A), whereas subtle structural differences, such as smaller fissures or cysts hidden from the macroscopic surface (Figure 1B), are not detected. This leads to overestimation of the quality of repair tissue by macroscopic assessment compared to histological measures (Figure 2).
Secondly, the lack of correlation could be explained by the introduction of individual judgement in the ICRS score, because both the degree of defect fill and measurement of the demarcating border require the observer to determine quantitative values based on individual estimations. It could be possible that repeated individual scoring results in a different score. Previous articles did not specify the degree of experience with the ICRS scoring of the observers, but one article did show a significant increase in inter observer agreement after 2 months training [30]. Whether this also influences the correlation to histology remains to be investigated.
Thirdly, the ICRS does not allow the observer to report graft hypertrophy, nor does it include the colour aspect of the defect. Both items have been discussed in literature to be of relative importance and are included in the Oswestry Arthroscopy scale. However, we were not able to detect a colour difference as used by the OAS (pearly hyaline-like, white fibrous tissue, yellow bone) between our samples with a good or a poor O’Driscoll score, since all were more or less white fibrous tissue.
Moreover, the O’Driscoll score assesses the borders in one plane and is location dependent, while the ICRS score takes the entire defect rim into consideration and judges the percentage of the rim that is attached. This explanation is supported by the fact that no correlation was found between the sub item scores for the integration of the repair tissue into the border zone.
The results indicate that despite the satisfactory inter observer reliability found previously, ICRS scoring may not be an accurate manner to determine cartilage or repair quality during arthroscopy. Arthroscopy also allows for assessment of multiple domains such as the size of the lesion and the general state of degeneration of the joint. Since these are all features that influence the healing or possible deterioration of cartilage defects, these items could be added in the score. to make the ICRS scoring more accurate [27,31-33].
For research purposes, alternatives of histology that are more accurate, precise and reliable should be considered, such as dGEMERIC and T2 mapping MRI, contrast enhanced CT or optical coherence tomography (OCT) [34]. These techniques are also applied more and more in clinical practice and according to the increasing amount of literature of these advanced techniques image parameters correlate highly with cartilage quality [35-38].
In conclusion, this animal study suggests that isolated macroscopic assessment of the quality of cartilage repair tissue of talar osteochondral defects treated with micro fracture using the ICRS score has a poor correlation with histological analysis. Possible explanations may be found in the limitations of surface assessment compared to analysis deeper into the tissue and the necessity of more elaborate macroscopic assessment including hypertrophy, colour, lesion size, location and degenerative status of the joint.
Acknowledgement
This work was supported by the Technology Foundation STW, Applied Science Division of NWO, and the technology program of the Ministry of Economic Affairs, The Netherlands and the Marti Keuning Eckhardt Foundation, Lunteren, the Netherlands. No conflict of interest was reported for any of the authors.
References
References
- id="Reference_Titile_Link" value="1">Hoemann CKR, Roberts S, Saris DBF, Creemers L, Mainil-Varlet P, et al. (2011) International Cartilage Repair Society (ICRS) recommended guidelines for histological endpoints for cartilage repair studies in animal models and clinical trials. Cartilage 2: 153-172.
- id="Reference_Titile_Link" value="2">Blackburn WD, JrChivers S, Bernreuter W (1996) Cartilage imaging in osteoarthritis.Semin Arthritis Rheum 25: 273-281.
- id="Reference_Titile_Link" value="3">Chevrier A, Hoemann CD, Sun J, Buschmann MD (2007) Chitosan-glycerol phosphate/blood implants increase cell recruitment, transient vascularization and subchondral bone remodeling in drilled cartilage defects. Osteoarthritis Cartilage 15: 316-327.
- id="Reference_Titile_Link" value="4">Arøen A, Heir S, Løken S, Engebretsen L, Reinholt FP (2006) Healing of articular cartilage defects. An experimental study of vascular and minimal vascular microenvironment.J Orthop Res 24: 1069-1077.
- id="Reference_Titile_Link" value="5">Milano G, SannaPassino E, Deriu L, Careddu G, Manunta L, et al. (2010) The effect of platelet rich plasma combined with microfractures on the treatment of chondral defects: an experimental study in a sheep model.Osteoarthritis Cartilage 18: 971-980.
- id="Reference_Titile_Link" value="6">Verhagen RA, Maas M, Dijkgraaf MG, Tol JL, Krips R, et al. (2005) Prospective study on diagnostic strategies in osteochondral lesions of the talus. Is MRI superior to helical CT?J Bone Joint Surg Br 87: 41-46.
- id="Reference_Titile_Link" value="7">Jackson DW, Lalor PA, Aberman HM, Simon TM (2001) Spontaneous repair of full-thickness defects of articular cartilage in a goat model. A preliminary study.J Bone Joint Surg Am 83-83A: 53-64.
- id="Reference_Titile_Link" value="8">Simon TM, Aberman HM (2010) Cartilage regeneration and repair testing in a surrogate large animal model.Tissue Eng Part B Rev 16: 65-79.
- id="Reference_Titile_Link" value="9">DelleSedie A, Riente L, Bombardieri S (2008) Limits and perspectives of ultrasound in the diagnosis and management of rheumatic diseases.Mod Rheumatol 18: 125-131.
- id="Reference_Titile_Link" value="10">Giannini S, Buda R, Grigolo B, Bevoni R, Di Caprio F, et al. (2010) Bipolar fresh osteochondral allograft of the ankle.Foot Ankle Int 31: 38-46.
- id="Reference_Titile_Link" value="11">Adachi N, Deie M, Nakamae A, Ishikawa M, Motoyama M, et al. (2009) Functional and radiographic outcome of stable juvenile osteochondritisdissecans of the knee treated with retroarticular drilling without bone grafting.Arthroscopy 25: 145-152.
- id="Reference_Titile_Link" value="12">Gikas PD, Morris T, Carrington R, Skinner J, Bentley G, et al. (2009) A correlation between the timing of biopsy after autologous chondrocyte implantation and the histological appearance.J Bone Joint Surg Br 91: 1172-1177.
- id="Reference_Titile_Link" value="13">Brun P, Dickinson SC, Zavan B, Cortivo R, Hollander AP, et al. (2008) Characteristics of repair tissue in second-look and third-look biopsies from patients treated with engineered cartilage: relationship to symptomatology and time after implantation.Arthritis Res Ther 10: R132.
- id="Reference_Titile_Link" value="14">Mithoefer K, McAdams T, Williams RJ, Kreuz PC, Mandelbaum BR (2009) Clinical efficacy of the microfracture technique for articular cartilage repair in the knee: an evidence-based systematic analysis.Am J Sports Med 37: 2053-2063.
- id="Reference_Titile_Link" value="15">Brittberg M, Winalski CS (2003) Evaluation of cartilage injuries and repair.J Bone Joint Surg Am 85-85A: 58-69.
- id="Reference_Titile_Link" value="16">Knutsen G, Drogset JO, Engebretsen L, Grøntvedt T, Isaksen V, et al. (2007) A randomized trial comparing autologous chondrocyte implantation with microfracture. Findings at five years.J Bone Joint Surg Am 89: 2105-2112.
- id="Reference_Titile_Link" value="17">Smith GD, Taylor J, Almqvist KF, Erggelet C, Knutsen G, et al. (2005) Arthroscopic assessment of cartilage repair: a validation study of 2 scoring systems.Arthroscopy 21: 1462-1467.
- id="Reference_Titile_Link" value="18">Brittberg M, Peterson L (1998) Introduction of an articular cartilage classification. ICRS Newsletter: 5-8.
- id="Reference_Titile_Link" value="19">Lee KB, Bai LB, Yoon TR, Jung ST, Seon JK (2009) Second-look arthroscopic findings and clinical outcomes after microfracture for osteochondral lesions of the talus.Am J Sports Med 37: 63S-70S.
- id="Reference_Titile_Link" value="20">Nakamura T, Sekiya I, Muneta T, Hatsushika D, Horie M, et al. (2012) Arthroscopic, histological and MRI analyses of cartilage repair after a minimally invasive method of transplantation of allogeneic synovial mesenchymal stromal cells into cartilage defects in pigs.Cytotherapy 14: 327-338.
- id="Reference_Titile_Link" value="21">van den Borne MP, Raijmakers NJ, Vanlauwe J, Victor J, de Jong SN, et al. (2007) International Cartilage Repair Society (ICRS) and Oswestry macroscopic cartilage evaluation scores validated for use in Autologous Chondrocyte Implantation (ACI) and microfracture.Osteoarthritis Cartilage 15: 1397-1402.
- id="Reference_Titile_Link" value="22">Kok AC, Tuijthof GJ, den Dunnen S, van Tiel J, Siebelt M, et al. (2013) No effect of hole geometry in microfracture for talarosteochondral defects.ClinOrthopRelat Res 471: 3653-3662.
- id="Reference_Titile_Link" value="23">O'Driscoll SW, Marx RG, Beaton DE, Miura Y, Gallay SH, et al. (2001) Validation of a simple histological-histochemical cartilage scoring system.Tissue Eng 7: 313-320.
- id="Reference_Titile_Link" value="24">Pineda S, Pollack A, Stevenson S, Goldberg V, Caplan A (1992) A semiquantitative scale for histologic grading of articular cartilage repair.ActaAnat (Basel) 143: 335-340.
- id="Reference_Titile_Link" value="25">Moojen DJ, Saris DB, Auw Yang KG, Dhert WJ, Verbout AJ (2002) The correlation and reproducibility of histological scoring systems in cartilage repair.Tissue Eng 8: 627-634.
- id="Reference_Titile_Link" value="26">Yoon CH, Kim HS, Ju JH, Jee WH, Park SH, et al. (2008) Validity of the sonographic longitudinal sagittal image for assessment of the cartilage thickness in the knee osteoarthritis.ClinRheumatol 27: 1507-1516.
- id="Reference_Titile_Link" value="27">Fleiss JL, Levin B, Paik MC (2004) The measurement of interrater agreement. statistical methods for rates and proportions: John Wiley & Sons, Inc. pp. 598-626.
- id="Reference_Titile_Link" value="28">Hattori K, Ikeuchi K, Morita Y, Takakura Y (2005) Quantitative ultrasonic assessment for detecting microscopic cartilage damage in osteoarthritis.Arthritis Res Ther 7: R38-46.
- id="Reference_Titile_Link" value="29">Batiste DL, Kirkley A, Laverty S, Thain LM, Spouge AR, et al. (2004) Ex vivo characterization of articular cartilage and bone lesions in a rabbit ACL transection model of osteoarthritis using MRI and micro-CT.Osteoarthritis Cartilage 12: 986-996.
- id="Reference_Titile_Link" value="30">Ayral X, Gueguen A, Ike RW, Bonvarlet JP, Frizziero L, et al. (1998) Inter-observer reliability of the arthroscopic quantification of chondropathy of the knee.Osteoarthritis Cartilage 6: 160-166.
- id="Reference_Titile_Link" value="31">Chuckpaiwong B, Berkson EM, Theodore GH (2008) Microfracture for osteochondral lesions of the ankle: outcome analysis and outcome predictors of 105 cases.Arthroscopy 24: 106-112.
- id="Reference_Titile_Link" value="32">Giannini S, Vannini F (2004) Operative treatment of osteochondral lesions of the talar dome: current concepts review.Foot Ankle Int 25: 168-175.
- id="Reference_Titile_Link" value="33">Becher C, Driessen A, Hess T, Longo UG, Maffulli N, et al. (2010) Microfracture for chondral defects of the talus: maintenance of early results at midterm follow-up.Knee Surg Sports TraumatolArthrosc 18: 656-663.
- id="Reference_Titile_Link" value="34">Kokkonen HT, Jurvelin JS, Tiitu V, Toyras J (2011) Detection of mechanical injury of articular cartilage using contrast enhanced computed tomography. Osteoarthritis Cartilage 19: 295-301.
- id="Reference_Titile_Link" value="35">Watanabe A, Boesch C, Anderson SE, Brehm W, Mainil Varlet P (2009) Ability of dGEMRIC and T2 mapping to evaluate cartilage repair after microfracture: a goat study.Osteoarthritis Cartilage 17: 1341-1349.
- id="Reference_Titile_Link" value="36">Bekkers JE, Bartels LW, Benink RJ, Tsuchida AI, Vincken KL, et al. (2013) Delayed gadolinium enhanced MRI of cartilage (dGEMRIC) can be effectively applied for longitudinal cohort evaluation of articular cartilage regeneration.Osteoarthritis Cartilage 21: 943-949.
- id="Reference_Titile_Link" value="37">Cernohorsky P, Kok AC, Bruin DM, Brandt MJ, Faber DJ, et al. (2015) Comparison of optical coherence tomography and histopathology in quantitative assessment of goat talus articular cartilage.ActaOrthop 86: 257-263.
- id="Reference_Titile_Link" value="38">Smith TO, Drew BT, Toms AP, Donell ST, Hing CB (2012) Accuracy of magnetic resonance imaging, magnetic resonance arthrography and computed tomography for the detection of chondral lesions of the knee.Knee Surg Sports TraumatolArthrosc 20: 2367-2379.
Tables and Figures at a glance
 |
|
|
| Table 1 | Table 2 | Table 3 |
Figures at a glance
 |
 |
| Figure 1 | Figure 2 |
Relevant Topics
Recommended Journals
Article Tools
Article Usage
- Total views: 14421
- [From(publication date):
September-2015 - Dec 21, 2024] - Breakdown by view type
- HTML page views : 9879
- PDF downloads : 4542
