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Final Thesis.Pdf Viral Hepatitis C Associated Neurocognitive Dysfunction in Ireland in the Direct-Acting Antiviral (DAA) Era Orla Strahan BA (Psychology), M.Sc. (Neuroscience), PGCert (Statistics) Thesis presented to the School of Psychology, University of Dublin, Trinity College, for the degree of Doctor of Philosophy Supervised by Dr. Paul Dockree and Dr. Robert Coen August 2020 Declaration I declare that this thesis has not been submitted as an exercise for a degree at this or any other university and it is entirely my own work. I agree to deposit this thesis in the University’s open access institutional repository or allow the Library to do so on my behalf, subject to Irish Copyright Legislation and Trinity College Library conditions of use and acknowledgement. I consent to the examiners retaining a copy of the thesis beyond the examining period, should they so wish (EU GDPR May 2018). Signed: ______________________________ Date: _________________ Orla Strahan i Acknowledgements First, I would like to sincerely thank my PhD supervisors, Dr. Robert Coen and Dr. Paul Dockree. I am eternally grateful to you for the support, guidance, and encouragement you have given me over the past three years. I also want to extend this gratitude to the Principal Investigator of The CANDI* Project, Prof. SuZanne Norris, who has taught me so much and will always be a role model I look up to. Additionally, I want to thank all the other co-supervisors and co-applicants on The CANDI Project all of whom provided valuable feedback, support and guidance to me. I would also like to specially thank Dr. Damien Ferguson, who has been a great friend and colleague over the past three years. I’ve learned a lot from you and I will always be grateful for sharing my PhD journey with you. A huge thanks also to Philip O’Gorman and Sara Naimimohasses for your friendship and everything you have done, and of course, a big thank you to all the wonderful research assistants, in particular, Angela Wu, who played a huge part in many aspects of this thesis. This project could not have been carried out without the involvement of the wonderful Hepatology and GUIDE staff in St. James’s Hospital, Dublin. From day one, you all took me in as part of your team, and I will always be grateful for the invaluable experience you have provided me. I also want to thank the Division of Neuropsychology in the Psychological Society of Ireland and the family of Dr. Deirdre McMackin. In 2017, I was awarded the Deirdre McMackin Memorial Award for my work on this project. Not only was this award able to fund an international conference and additional materials, but it also gave me a much needed sense of confidence in my research and in my future career prospects. Lastly, I want to thank my partner Paul, who has shown unlimited love and support through this journey; my mother, who has selflessly put my education first, and none of my achievements would have been possible without you; The rest of my family – my sister Aoife, my aunts Bridann and Hilda, and my uncles Thomas and John; and to all my friends who have supported me, in particular, Lauren, Sarah, Megan, Aoife and Aoife. *The CANDI Project, funded by the Health Research Board (HRB) of Ireland, was a large study exploring the nature of neurocognitive dysfunction in individuals living with chronic Hepatitis C in Ireland. This was explored through different disciplines, including psychology, neurology, and physiotherapy. The studies forming the basis of this thesis focuses on the psychology aspect of The CANDI Project and was undertaken during a PhD studentship funded through The CANDI Project. The neurology aspects were investigated by D. F. (PhD Candidate, School of Medicine, Trinity College Dublin), and the exercise physiotherapy aspects were investigated by P. O’G (PhD Candidate, Discipline of Physiotherapy, Trinity College Dublin). ii Summary Neurocognitive dysfunction is common in the setting of cirrhosis and hepatic encephalopathy in patients infected with the Hepatitis C Virus (HCV). However, neurocognitive dysfunction has also been described in non-cirrhotic patients with HCV and there are reports of HCV encroachment in the central nervous system (CNS) (Forton et al., 2001, 2002). HCV is thought to be introduced to the CNS by either direct viral invasion or indirect neuroinflammation. Neurological abnormalities have been reported in regions such as the prefrontal cortex (PFC), basal ganglia, thalamus, and white matter tracts (Forton et al., 2002; McAndrews et al., 2005; Weissenborn et al., 2004). Dysfunction to these fronto-striatal circuits are thought to be responsible for the difficulties observed in memory, attention, processing speed, and executive functions. However, there is wide variation in the reported prevalence of HCV-associated neurocognitive dysfunction (HCV-AND). Additionally, HCV is associated with numerous extra- hepatic manifestations including mood disturbances, fatigue, and reduced health-related quality of life (HRQoL) (Younossi, Park, Henry, et al., 2016), which may negatively impact neurocognitive functioning. Furthermore, previous research has suggested the possible reversibility of HCV-AND following viral eradication using interferon (INF)-based therapies (Byrnes et al., 2012). The findings are, however, mixed due in large part to the limitations associated with INF (e.g. low response rates, psychiatric side effects). The introduction of INF- free therapies in 2014, known as Direct-Acting Antivirals (DAAs), has revolutionised HCV treatment worldwide and has since become the standard treatment for chronic HCV infection. However, the reversibility of HCV-AND has not yet been investigated in the DAA-era in non- cirrhotic individuals. Therefore, the current thesis was designed to explore the nature of HCV- AND in an Irish sample of non-cirrhotic HCV positive individuals, as well as the potential impact of viral eradication, using DAAs, on neurocognitive functioning. The first study included in this thesis (Study 1, Chapter 3) aimed to characterise the profile of HCV-AND in 135 mono-infected, non-cirrhotic HCV positive individuals, using a number of neuropsychological test measures. All patients were recruited from outpatient liver clinics in St. James’s Hospital, Dublin. Of the sample, all of whom had been screened for evidence of cognitive problems, 83% demonstrated difficulties in one or more cognitive domain, including memory (encoding and retrieval but not in retention/storage), attention and executive functioning, and performance was influenced by factors such as lower education and previous substance abuse. The second study (Study 2a, Chapter 4) aimed to investigate the nature and extent of select extra- hepatic features of chronic HCV infection, including depression, anxiety, fatigue and HRQoL, in the same sample of individuals examined in Study 1. Low mood was prevalent in 41-64% of the sample, fatigue was prevalent in 73% and reduced HRQoL was prevalent in 20-33% of the iii sample. These symptoms were independent of disease-related characteristics, such as, genotype, viral load, degree of fibrosis, and years since diagnosis. In addition, low mood was found to impact negatively performance on memory tests. The third study (Study 2b, Chapter 4) aimed to control for confounding factors inherent in studies of HCV samples by investigating potential difference in neuropsychological performance and mood state between a chronic HCVRNA positive group and a HCVRNA negative group. The HCVRNA positive group was studied as part of the larger research project and for whom screening data were available (n = 709), and the HCVRNA negative group were a specially recruited sample of individuals who, following infection, spontaneously cleared the virus (n = 32). HCVRNA positive individuals were four times more likely to demonstrate impaired performance on the brief cognitive screening test when compared to HCVRNA negative individuals. In addition, both groups reported similarly high levels of mood disturbances, suggesting that HCV-AND is independent of low mood. The final study (Study 3, Chapter 5) was a follow-up of those individuals included in Study 1. The aim of this study was to determine the effects of HCV viral eradication using DAAs on HCV- AND and the selected extra-hepatic manifestations. Following baseline assessment (Study 1), individuals enrolled in a 6 month intervention, where they were randomised to either a treatment group (DAA group) or a Control group. 96 individuals returned for follow-up assessment. 54 individuals received DAA treatment and successfully cleared the virus (DAA group), and 42 underwent routine care (Control group). Following successful viral eradication, significant improvements were observed in memory, attention, executive functions and visuospatial abilities. In general, these improvements were not observed for the Control group, although there was evidence of a practice effect on a number of tests. At follow-up, there were some improvements observed in both the DAA and the Control group in terms of mood but the prevalence of mood issues still remained considerably high. In conclusion, the results of this thesis demonstrates the presence of neurocognitive difficulties among non-cirrhotic HCVRNA positive individuals. Although mild, these neurocognitive difficulties are complex and can be influenced by socioeconomic factors. Additionally, extra- hepatic manifestations, including low mood, fatigue and HRQoL are highly prevalent and may further complicate HCV-AND, Furthermore, these results extend the benefits of DAAs beyond the liver through the improvement in HCV-AND following successful viral eradication. However, the impact of viral eradication on extra-hepatic manifestations remains unclear, and they may persist following viral clearance. iv Conference Presentations Strahan, O., Ferguson, D., Coen, R., Dockree, P., Doherty, C., O’Gorman, P., Gormley, J., Mckiernan, S., Bergin, C., Norris, S. and the CANDI Authors’ Group. (2019). Reversal of Neurocognitive Dysfunction in Non-Cirrhotic HCV Infected Patients; Impact of DAA’s Beyond the Liver. Poster presented at the American Association for the Study of Liver Disease (AASLD) Annual Liver Meeting, Boston, Massachusetts, USA, Nov 8-12th 2019.
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