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The Biology of Cartilage

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The Biology of Cartilage 1 Factors affecting outcome after autologous chondrocyte implantation for the treatment of osteochondral defects of the knee By Parag Kumar Jaiswal BSc, MBBS, FRCS(T&O). Revised thesis submitted for the degree of Doctor of Medicine MD(Res). October 2014 The Royal National Orthopaedic Hospital Trust and The Institute of Orthopaedics and Musculoskeletal Science, University College London 2 ABSTRACT Some studies on autologous chondrocyte implantation (ACI) have demonstrated little benefit over other techniques and few have demonstrated a lasting benefit. A number of factors can contribute to failure and a scientific approach to elucidate these variables has not been reported. This thesis reports on the use of a statistical approach - the Generalised Linear Model (GLM) to quantify the effect each factor has whilst considering the interplay of other variables. Data from a randomised controlled trial and several case-controlled studies will assess the efficacy of 2 different types of ACI, the influence of smoking, BMI, and physical activity. Non- modifiable risk factors that were assessed include the aetiology, site and size of the lesion, the duration of symptoms and number of previous operations prior to the index procedure and the presence of early osteoarthritis. Site had a significant effect on outcome but size did not. The GLM predicted a point increase in the Modified Cincinnati Score (MCS) before surgery (MCS 0) would lead to a further 0.5 point increase in MCS 2 years postoperatively (MCS 24) (p=0.001). Other significant non- modifiable risk factors include age and sex of the patient. When treating lesions in the patella, duration of symptoms was a significant factor, but age was not. 3 The GLM predicted that smokers’ MCS 24 (the Modified Cincinnati Score 2 years after surgery) was likely to be 15 less than non-smokers (p=0.002). Patients playing no sports experienced an 11.4 point decrease. For each increase in BMI, the MCS 24 was 2.4 less (p=0.001). Factors that optimise outcome following surgery are; avoidance of numerous procedures prior to ACI and delay of more than one year before undergoing ACI. Current NICE guidelines prohibit the use of ACI as the first-line surgical procedure and prevent addressing the above 2 issues. Poorer results were observed in obese patients. Weight loss and active lifestyle are essential pre-operatively. Furthermore, we recommend that pre-operative counselling for smokers is essential and that all smokers be offered a cessation programme. 4 DECLARATION I declare that this is a group of patients that have been referred to and treated by The Royal National Orthopaedic Hospital Trust. All these patients have been treated following a local research ethical committee application (reference No 981028), and a multi-centre research committee application for the study of autologous cartilage cell implantation (ACI-C) compared with membrane carried cartilage cell implantation (MACI) for treatment of damaged cartilage lining of the knee (reference No 02/01/73). Professor George Bentley has been the principal investigator for these studies. Specific Contribution To The Work When I started in the research post, 691 procedures had been performed in the Joint Reconstruction Unit at The Royal National Orthopaedic Hospital as either part of a randomised controlled trial (RCT) or a prospective cohort study. When reporting on the RCT, there was missing data which I retrieved whilst also ensuring that new patients had adequate data collection. Specifically, out of 247 consecutive patients that had either an ACI or matrix- carried autologous chondrocytes implantation (MACI) procedure performed in a 3 year period, only 137 patients had functional scores recorded 2 years after surgery. I managed to get the latest functional scores in a further 69 patients. This was also true for the patients in chapter 4 when assessing the efficacy of autologous chondrocytes implantation (ACI) in the patella-femoral joint. In chapter 5, I reviewed all 200 radiographs and also retrieved missing data. A colleague also reviewed 115 radiographs so that we could perform inter-observer error for two different types of radiographic scoring 5 systems. The work in chapter 6 was entirely my own. I created the new data capture form for smoking status, body mass index (BMI) and physical activity. I distributed the forms and collected data. I certify that the work in this thesis is original, though the collection of data has been supported by others and will be acknowledged accordingly. The analysis of data and subsequent conclusions are entirely the work of the author. Further my research has been conducted ethically and the results are genuine. Parag K. Jaiswal 6 ACKNOWLEDGEMENTS My deepest gratitude goes towards Professor G. Bentley and Professor D. Marsh. Professor Bentley initially stimulated my interest in this subject and has been my mentor throughout. Professor Marsh has taught me the virtues of approaching a problem with a keen scientific mind. Without the help of both professors this thesis would not have been possible. I would like to thank my preceding research fellow Derek Park for acting as an independent observer in one of the chapters, and also Simon Macmull whose help was invaluable in helping retrieve missing data. I am also indebted to my co-supervisor, Caroline Dore and her colleague Suzie Cro for their statistical advice. Finally, the journey to complete this thesis was long and arduous but made significantly easier with the love, support and patience of my wife, Roopa and my children Eva and Kara. I am sorry so much time was spent away from you! They say that behind every successful man there stands a woman; I am very fortunate to have one extraordinary woman and two beautiful girls who inspire me to greater heights.... 7 Contents Title Page 2 Abstract 3-4 Declaration 5 Specific contribution to work 5-6 Acknowledgements 7 List of tables and figures 12-16 List of abbreviations 17-18 Chapter 1: The Biology of Cartilage Introduction 19-47 Composition 19-26 Structure 27-32 Injury 33-38 Treatment of Cartilage Injuries 39-45 Autologous Chondrocyte Implantation 46-47 Goals of this Thesis 48-49 Chapter 2: Methods 50-63 Introduction 50 Outline of patients 50-52 The Modified Cincinnati Score 53-57 Statistical Approach 57-63 8 Chapter 3: Autologous Chondrocyte Implantation using Type I/III Collagen Membrane (ACI-C) vs Matrix-Carried Autologous Chondrocyte Implantation (MACI) Introduction 64-68 Operative Technique 69-74 Aims and Objectives 75 Patients and Methods 76-80 Results 81-102 Discussion 103-110 Chapter 4: The Treatment of Patellofemoral Osteochondral Defects Introduction 111-120 Aims and Objectives 120 Patients and Methods 121-122 Results 123-138 Discussion 139-143 Chapter 5: Radiographic Evidence of Osteoarthritis Introduction 144-149 Aims and Objectives 150 Patients and Methods 151-155 Results 156-170 Discussion 171-176 9 Chapter 6: Smoking, Body Mass Index and Physical Activity Introduction 177-184 Smoking 179 Body Mass Index 180-181 Physical Activity 182-184 Aims, Objectives and Hypotheses 185 Patients and Methods 186-187 Results 188-211 Smokers 188-194 Body Mass Index 195-201 Physical Activity 202-204 Generalised Linear Model 205-207 Generalised Linear Model – Further Variables 208-211 Discussion 212-225 Smoking 214-216 Body Mass Index 217-220 Physical Activity 221-223 What can be done? 224-225 10 Chapter 7: Discussion Methodological Considerations 226-229 Main Findings 230-231 Clinical Consequences 232-234 Limitations 235-237 Future Direction 238-244 Conclusion 244 References 245-270 Appendices Appendix I: 271-286 Data Collection Proforma for ACI-C vs MACI study Appendix II: 287-292 Data Collection Proforma for Chapter 6: Smoking, BMI, and Physical Activity 11 List of tables and figures Chapter 1 Introduction P. 22 Figure 1.1: Immunochemical localization of type II collagen in an intact articular cartilage region from the knee joint. P. 24 Figure 1.2: The micrograph shows a portion of an aggregate isolated from cartilage that consists of a central filament of hyaluronan and a large number of attached monomer (aggrecan) proteoglycans P. 26 Figure 1.3: Diagrammatic representation of the macrofibrillar collagen network and aggrecan with hyaluronic acid P. 27 Figure 1.4: The zones of articular cartilage P. 28 Figure 1.5: Diagrammatic representation of articular cartilage P. 31 Figure 1.6: Functions of Hyaline cartilage and matrix Chapter 2: Methods P.54 Table 2.1: The Modified Cincinnati Score Chapter 3: ACI-C vs MACI P.69 Figure 3.1: Harvesting of cartilage graft P.70 Figure 3.2: Overview of ACI-C (Second Stage) P.71 Figure 3.3: Debrided cartilage defect seen intra-operatively P.71 Figure 3.4: The collagen type I/III membrane is sutured to the defect and the cultured chondrocytes are injected P.72 Figure 3.5: Template cut to size and syringe containing fibrin glue P.73 Figure 3.6: Final appearance of MACI graft P.74 Figure 3.7: Overview of MACI 12 P.79 Figure 3.8: CONSORT statement P.81 Table 3.1: Patient and lesion characteristics P.82 Figure 3.9: Age distribution of patients P.82 Table 3.2: Anatomical site of chondral lesions according to treatment groups P.83 Table 3.3: Aetiology of lesions according to treatment groups P.83 Figure 3.10: The Modified Cincinnati Scores P.84 Figure 3.11: Change in Modified Cinicinnati Scores (MCS) from baseline P.86 Figure 3.12: Timelines for patients undergoing ACI and MACI P.87 Table 3.4: Proportion of Excellent and Good Results in ACI and MACI patients P.88 Table 3.5: A comparison
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