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Upgrade Planning The relationship between nutritional and inflammatory changes during critical illness A thesis submitted for the degree of Doctor of Philosophy Imperial College London By Liesl Wandrag Section of Investigative Medicine Division of Endocrinology, Diabetes and Metabolism Faculty of Medicine Imperial College London July 2013 1 Abstract Muscle mass loss in the critically ill is substantial, between 1-2% per day. Muscle wasting and weakness delays patient recovery and rehabilitation. Understanding the relationship between nutritional and inflammatory markers will help to identify a notional “nutritional tipping point”, where anabolism exceeds catabolism, which will allow us to target nutritional therapy more successfully. Muscle depth on ultrasound, inflammatory markers, cytokines, urinary markers of protein breakdown and nitrogen balance data were collected in 78 critically ill patients. Patients lost a significant amount of muscle depth during their intensive care unit (ICU) stay. Results indicate that a nutritional tipping point is unlikely to exist during an ICU admission. Data suggests that nitrogen balance remains negative over 20 days, indicating that whilst patients should continue to receive standard nutrition support during their ICU stay, any additional nutritional strategy should be targeted outside of the ICU environment. Multilevel modelling indicated that each additional day spent on ICU was significantly associated with decreased C-reactive protein, muscle depth and interleukin-10 levels. With every year increase in a patient’s age muscle depth and 3-methylhistidine levels were significantly reduced and interleukin- 10 levels were significantly increased. Sample size estimates from current data provide some guidance for future studies, however estimates should be viewed with caution. The feasibility of providing a leucine-enriched essential amino acid supplement to trauma ICU patients was furthermore assessed. Inflammatory and nutritional makers were assessed along with protein turnover. Although it was feasible to use the supplement in the trauma population, studying this patient group was more complicated than anticipated. Whole body protein turnover was enhanced in trauma patients with breakdown far exceeding synthesis. These studies suggest that although it may be feasible to provide amino acid supplementation to critically ill patients, this type of intervention should be targeted outside of the ICU environment. 2 Statement of work The majority of the work described in this thesis was performed by the author. Collaborations are listed in the acknowledgements. Assistance provided is described below: Chapter 4: Recruitment and data collection at St Mary’s Hospital was performed by Ms Ella Segaran whilst I was recruiting at Charing Cross and Hammersmith Hospitals for the Nutritional Tipping Point study. ICU Research nurses from Imperial College Healthcare NHS Trust assisted with screening and some of the patient recruitment. Ms May To continued to recruit patients and collect data at other sites once I started recruiting for the essential amino acid study at Kings College Hospital. Ms May To performed the ELISA for cytokine analysis. Chapter 5: ICU research nurse at Kings College Hospital London assisted with screening of patients. Ms May To performed the ELISA for cytokine analysis for the essential amino acid supplementation study. All stable isotope studies were performed with the assistance of two ICU research nurses. Statistical Analysis: Reliability statistics, descriptive statistics and sample size estimates were performed by me. The multilevel modelling in Chapter 4 was performed by a statistician. 3 Acknowledgements I am incredibly grateful to my three supervisors, Dr Stephen Brett for his invaluable clinical expertise and unwavering support throughout this project, and Dr Mary Hickson and Prof Gary Frost for their exceptional academic support over the years. Their guidance and encouragement has been inspirational. I am enormously grateful to my funder: The Department of Health via the National Institute for Health Research (NIHR) for providing me with a Clinical Doctoral Research Fellowship. Support of the National Institute for Health Research, through the Comprehensive Clinical Research Network should also be acknowledged. I am grateful to Ms Ella Segaran and Ms May To for screening and recruiting for the nutritional tipping point study and to Ms To who conducted all the cytokine analysis (ELISA) under supervision of Dr Fred Tam, Imperial College London. I am very grateful for the support and guidance that Dr Tam provided during this analysis. All Critical Care clinical, research and audit staff at both Imperial College Healthcare NHS Trust and Kings College Hospital are acknowledged for support throughout this research. At Kings College Hospital the bedside nurses administered the amino acid supplement. I am very grateful in particular to the critical care research and clinical audit team from both Imperial College Healthcare NHS Trust and Kings College Hospital Trust. Without the input and support of the research nurses this study would have been very difficult to complete. Thank you in particular to research nurse Juan Moreno at Hammersmith Hospital who assisted with screening and recruitment on days when I had study patients elsewhere. Research nurses in Critical Care and the Emergency Department at Kings College Hospital are thanked for their assistance with screening and with unwavering support in performing the stable isotope studies, in particular infusion preparation, blood sampling and assistance with gas sampling via the Douglas bag. Support and advice from Critical Care Consultants at Kings College Hospital, in particular Dr Stephanie Strachan, Dr Phil Hopkins, Dr Andre Vercueil and Dr Ritesh Maharaj. I would like to thank laboratory staff at Charing Cross Hospital for all the urinary analysis, in particular Maribel Gracia under guidance of Dr Maggie Hancock. I would also like to thank staff at the Institute of Liver Studies, Kings College Hospital for use of freezer space and assistance with dry ice provision for sample transfer. I am very grateful to Dr Nicola Jackson, Mrs Jo Batt, Dr Martin Whyte, Dr Moradie and Prof Margot Umpleby at Surrey University for support and guidance with stable isotope study preparation and analysis. 4 Also, thank you to Claire Black, NIHR Clinical Doctoral Research Fellow at UCL, for her invaluable input into indirect calorimetry at the start of this project. I would like to acknowledge support from the SHS/Nutricia (Nutricia Ltd., Wiltshire, United Kingdom) for provision of the essential amino acid and leucine supplements. I would like to thank and acknowledge support from the statistical service at University College London (UCL) for multilevel modelling analysis of the nutritional tipping point study, performed by Ms Bountziouka and Dr Wade. Last but not least, thank you to my family and friends for their love, support and patience over the years. In particular, to my husband David for your support, astute advice, for cooking and for generally putting up with it all! 5 Copyright declaration The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution-Non Commercial-No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or distribution, researchers must make clear to others the licence terms of this work. 6 Table of Contents Chapter 1. Introduction ...................................................................................................... 21 1. 1 Muscle mass ................................................................................................................ 22 1.1.1 Muscle mass in health ........................................................................................... 22 1.1.2 Muscle mass in critical illness ................................................................................ 23 1.2 Skeletal muscle mass control ........................................................................................ 24 1.2.1 Skeletal muscle breakdown and synthesis ............................................................ 24 1.3 Skeletal muscle breakdown .......................................................................................... 26 1.3.1 The stress response .............................................................................................. 26 1.3.2 Neuro-endocrine response .................................................................................... 27 1.3.3 Cytokines and muscle breakdown ......................................................................... 28 1.3.4 Signalling pathways regulating muscle breakdown ............................................... 30 1.3.5 Hypoxia, inflammation and wasting ....................................................................... 32 1.3.6 Reactive oxygen species (ROS) and nitric oxide (NO) .......................................... 34 1.3.7 Age ......................................................................................................................... 34 1.3.8 Drugs...................................................................................................................... 34 1.3.9 Immobility and disuse atrophy ..............................................................................
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