ptc.2023.75.issue-1

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Physiotherapy Canada Advancing health through scientific inquiry and knowledge translation Pour l’avancement de la santé par l’enquête scientifique et la transmission du savoir Volume 75 • Number 1  February 2023  ISSN 0300-0508  E-ISSN 1708-8313 TABLE OF CONTENTS 1 Current Practice, Barriers to, and Facilitators of Exercise Testing and Training by Physiotherapists in Cystic Fibrosis Specialized Centres in ORIGINAL RESEARCH Canada S. Malik, B. Levi, A. Chan, H. Cotnam, L. Martineau, E. Thieu, K. Zabjek, © Canadian Physiotherapy Association, 2023 P. Sisodia, and K. Wu 10 Clinician’s Commentary L. Wickerson 12 Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors: A Systematic Review and Meta-Analysis P.S. Akbari, Y. Hassan, L. Archibald, T. Tajik, K. Dunn, M. Berris, and J. Smith-Turchyn 22 Benefcial Effects of Preoperative Exercise on the Outcomes of Lumbar Fusion Spinal Surgery D.C. Lawrence, A. Montazeripouragha, E.K. Wai, D.M. Roffey, K.M. Phan, P. Phan, A. Stratton, S. Kingwell, G. McIntosh, A. Soroceanu, E. Abraham, C.S. Bailey, S. Christie, J. Paquet, A. Glennie, A. Nataraj, H. Hall, C. Fisher, Y.R. Rampersaud, K. Thomas, N. Manson, M. Johnson, and M. Zarrabian 29 Clinician’s Commentary T. Carter 30 A Meta-Analysis of Remote Ischemic Preconditioning in Lung Surgery and Its Potential Role in COVID-19 L.P. Cahalin, M.F. Formiga, J. Owens, and B.M. Osman 42 A Pan-Canadian Perspective on Education and Training Priorities for Physiotherapists. Part 1: Foundations for Clinical Practice M.J. Kleiner and D.M. Walton 53 Clinician’s Commentary S.C. Marshall 55 A Pan-Canadian Perspective on Education and Training Priorities for Physiotherapists. Part 2: Professional Interactions and Context of Practice M.J. Kleiner and D.M. Walton 65 Reliability and Validity of Shoulder and Handgrip Strength Testing N.R. Biasini, B. Bannon, M. Pellegrino, A. Qaderi, W. Trinh, S. Switzer-McIntyre, W.D. Reid, and K.T. Kasawara

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 PAEDIATRIC PHYSIOTHERAPY SERIES 72 Clinician’s Commentary L.V. Bonetti COCHRANE COLLABORATION INSTRUCTIONS FOR AUTHORS 74 Muscle Architecture and Subcutaneous Fat Measurements of Rectus Femoris and Vastus Lateralis at Optimal Length Aided by a Novel Ultrasound Transducer Attachment B.D. Bulbrook, J.N. Chopp-Hurley, E.G.Wiebenga, J.M. Pritchard, A.A. Gatti, P.J. Keir, and M.R. Maly 83 Development of the Gross Motor Function Family Report (GMF-FR) for Children with Cerebral Palsy P.S.C. Chagas, P. Rosenbaum, F.V. Wright, L. Pritchard, M. Wright, A.M. Toledo, A.C.R. Camargos, E. Longo, and H.R. Leite 92 Clinician’s Commentary L. Katchburian 94 What Does Cochrane Say About … Health Care Professional Education? 95 © Canadian Physiotherapy Association, 2023

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Physiotherapy Canada Advancing health through scientifc inquiry and knowledge translation Pour l’avancement de la santé par l’enquête scientifque et la transmission du savoir SCIENTIFIC CO-EDITORS EDITORIAL OFFICE Dina Brooks, PhD, MSc, BSc (PT) University of Toronto Press - Journals Division Professor, Vice-Dean & Executive Director 5201 Dufferin St., North York, ON M3H 5T8 Canada Tel.: 416- School of Rehabilitation Science, McMaster University, Hamilton, 667-7777 ext. 7751, Fax: 416-667-7832 or 1-800-221-9985, ON E-mail: [email protected], www.utpjournals.press Marilyn MacKay-Lyons, BSc(PT), MSc(PT), PhD INTERNATIONAL ADVISORY BOARD Professor, School of Physiotherapy, Dalhousie University, Halifax, NS Rik Gosselink, PhD, PT Professor, Department of Rehabilitation Sciences, Katholieke ASSOCIATE EDITORS Universiteit Leuven, Leuven University, Belgium Denise Connelly, PhD, BScPT Karen Grimmer-Somers, PhD, MMedSci, BPhty, CertHealthEc, Associate Professor, School of Physical Therapy, University of LMusA Western Ontario, London, ON Professor, School of Health Sciences Director, Centre for Allied Health Evidence, University of South Australia, Australia Isabelle Gagnon, pht, PhD Assistant Professor, School of Physical and Occupational Meg E. Morris, BAppSC(Physio), MAppSc, Grad Dip(Geron), Therapy, McGill University, Montreal, QC PhD, FACP Professor and Chair, School of Physiotherapy, University of S. Jayne Garland, PhD, PT Melbourne, Australia Professor and Department Head, Department of Physical Therapy, University of British Columbia, Vancouver, BC Kenneth J. Ottenbacher, OT, PhD Russel Shearn Moody Distinguished Chair in Neurological Crystal MacKay, PhD, PT Rehabilitation, Senior Associate Dean for Graduate Research Scientist, West Park Healthcare Centre Assistant Professor, Education, School of Allied Health Sciences, University of Texas Department of Physical Therapy, University of Toronto, ON Medical Branch, USA Maxi Miciak, PhD, PT Carol L. Richards, PhD, PT, FCAHS Adjunct Associate Professor, Faculty of Rehabilitation Medicine, Professor and Canada Research Chair in Rehabilitation, University of Alberta; Principal, Maxi Miciak Consulting, Department of Rehabilitation Medicine, Laval University, Quebec Edmonton, AB City, QC Kathleen E. Norman, BScPT, PhD Peter Rosebaum, MD, CM, FRCP(C) Associate Professor and Associate Director (Research and Post- Professor, Department of Pediatrics, McMaster University Professional Programs), School of Rehabilitation Therapy, Queen’s Hamilton, ON University, Kingston, ON Julius Sim, BA, MSc(Soc), MSc(Stat), PhD Brenda O’Neill, BScPT, Fellow HEA, PhD Primary Care Musculoskeletal Research Centre, Keele University, Centre for Health and Rehabilitation Technologies (CHART), UK Institute Nursing and Health Research, Sch Health Sciences, Ulster University, Northern Ireland STATISTICAL CONSULTANT Marco Pang, BScPT, PhD Paul Stratford, PT, MSc Assistant Professor, Department of Rehabilitation Sciences, The Professor Emeritus, School of Rehabilitation Science, McMaster Hong Kong Polytechnic University, Kowloon, Hong Kong University, Hamilton, ON Michelle Ploughman, PhD, PT PUBLISHER Associate Professor of Medicine and Canada Research Chair, Memorial University of Newfoundland, St. John’s, NL Canadian Physiotherapy Association 955 Green Valley Crescent, Suite 270, Ottawa, ON Didier Saey, pht, PhD K2C 3V4 Canada Professor, Faculty of Medicine, Université Laval, Quebec, QC Tel.: 613-564-5454 or 800-387-8679, Fax: 613-564-1577 E-mail: [email protected] www.physiotherapy.ca James Shaw, PT, PhD Scientist, Women’s College Hospital; Research Director and Competing Interest Statements for Physiotherapy Canada Assistant Professor, University of Toronto, Toronto, ON Editorial Board members are available online at https://www.utpjournals.press/journals/ptc/editorial-board Sarah Wojkowski, MScPT, PhD Associate Professor, Rehabilitation Science, McMaster University, Hamilton, ON © Canadian Physiotherapy Association, 2023

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 STATEMENT OF PURPOSE OBJECTIF Physiotherapy Canada is the official, scholarly, refereed journal of the Canadian Physiotherapy Association, giving direction to excellence in Physiotherapy Canada est la publication scientifique officielle révisée en clinical science and reasoning, knowledge translation, therapeutic skills profondeur de l’Association canadienne de physiothérapie. and patient-centred care. Son objectif est de fournir des orientations à l’excellence en sciences et en Recognized as one of the top five evidence-based journals of raisonnement clinique, transmission du savoir, compétences physiotherapy worldwide, Physiotherapy Canada publishes the results of thérapeutiques et soins centrés sur le patient. qualitative and quantitative research including systematic reviews, meta analyses, meta syntheses, public/health policy research, clinical practice Reconnu comme l’un des cinq grands journaux de physiothérapie guidelines, and case reports. Key messages, clinical commentaries, case reposant sur des faits scientifiques dans le monde, Physiotherapy Canada studies, evidence-based practice articles, brief reports, and book reviews publie les résultats de recherches qualitatives et quantitatives, notamment support knowledge translation to clinical practice. des revues systématiques, des méta-analyses, des métasyntheses, des recherches en politiques de la santé ou en politiques publiques, des Founded in 1923, Physiotherapy Canada meets the diverse needs of directives en pratique clinique et des études de cas. Ses messages clés, national and international readers and serves as a key repository of commentaires cliniques, études de cas, articles fondés sur des faits inquiries, evidence and advances in the practice of physiotherapy. scientifiques, résumés de discussions et comptes-rendus de livres favorisent la transmission du savoir à la pratique clinique. Physiotherapy Canada (ISSN 0300-0508) is published four times per year in Fspebrirnuga,rsyu, Mmamy,eAru, fgaullsta,nadndwNinotveermbbyetrhbeyUthneivUenrsiivteyrsoiftyTofronto Fondée en 1923, Physiotherapy Canada répond aux divers besoins de PTorerossntforPtrhesesCfoarntahdeiaCnanPahdyisainotPhheyrsaipotyhAersasopyciAastisoonc.iation. lecteurs canadiens et étrangers et se positionne comme un véritable recueil sur la recherche, les faits scientifiques et les progrès dans la EDITORIAL SUBMISSIONS pratique de la physiothérapie. Physiotherapy Canada welcomes manuscripts reporting results of qualitative or quantitative research. 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https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 ORIGINAL RESEARCH Current Practice, Barriers to, and Facilitators of Exercise Testing and Training by Physiotherapists in Cystic Fibrosis Specialized Centres in Canada Sarib Malik, MScPT, BHSc;*† Bella Levi, MScPT, BAHKin;*† Alan Chan, MScPT, MScHK, BScHK;† Hilary Cotnam, MScPT, BScHK;† Luc Martineau, MScPT, BHSc;† Eldon Thieu, MScPT, BSc Kin;† Karl Zabjek, PhD, MSc, BSc;†‡ Poonam Sisodia, BPT;§ Kenneth Wu, MBA, MA, BScPT†‡§ ABSTRACT Purpose: This study surveyed physiotherapists working at Canadian cystic fibrosis (CF) specialized centres to investigate the current practice, barriers to, and facilitators of exercise testing and training. Method: Physiotherapists were recruited from 42 Canadian CF centres.They responded to an e-questionnaire regarding their practice. The data were analyzed using descriptive statistics. Results: Eighteen physiotherapists responded (estimated response rate of 23%); median years of clinical experience was 15 (range, min-max, 3–30) years. Aerobic testing was administered by 44% of respondents, strength testing by 39%, aerobic training by 78%, and strength training by 67%. The most frequently reported barriers across all four types of exercise testing and training were insufficient funding (reported by 56%–67% of respondents), time (50%–61%) and staff availability (56%). More late career than early career physiotherapists reported utilizing aerobic testing (50% vs. 33% of respondents), strength testing (75% vs. 33%), aerobic training (100% vs. 67%), and strength training (100% vs. 33%). Conclusions: Exercise testing and training is underutilized in Canadian CF centres. Experienced physiotherapists reported utilizing exercise testing and training more than less-experienced physiotherapists. Post-graduate education and mentorship, especially for less- experienced clinicians, are recommended to emphasize the importance of exercise testing and training. Barriers of funding, time, and staff availability should be addressed to further improve quality of care. Key Words: cystic fibrosis; endurance training; professional practice gaps; rehabilitation; resistance training. RÉSUMÉ Objectif: sondage auprès de physiothérapeutes qui travaillent dans des centres canadiens spécialisés en fibrose kystique (FK) pour examiner les pratiques, les obstacles et les incitations actuels liés aux épreuves et aux entraînements à l’exercice. Méthodologie: les physiothérapeutes ont été recrutés dans 42 centres canadiens spécialisés en FK. Ils ont répondu à un questionnaire en ligne au sujet de leur pratique. Les données ont été analysées au moyen de statistiques descriptives. Résultats: les 18 physiothérapeutes qui ont répondu (taux de réponse estimatif de 23 %) avaient une médiane de 15 années d’expérience clinique (plage minimale-maximale de trois à 30 ans). Ainsi, 44 % des répondants effectuaient des épreuves d’endurance aérobique, 39 %, des épreuves en résistance, 78 %, un entraînement aérobique et 67 %, un entraînement en résistance. Les obstacles les plus signalés dans les quatre types d’épreuves et d’entraînement à l’exercice étaient un financement insuffisant (par 56 % à 67 % des répondants), le manque de temps (50 % à 61 %) et le peu de disponibilité du personnel (56 %). Plus de physiothérapeutes en fin de carrière qu’en début de carrière ont déclaré utiliser les épreuves d’endurance aérobique (50 % par rapport à 33 % des répondants), les épreuves de résistance (75 % par rapport à 33 %), l’entraînement aérobique (100 % par rapport à 67 %) et l’entraînement en résistance (100 % par rapport à 33 %). Conclusions: l’épreuve et l’entraînement à l’exercice sont sous-utilisés dans les centres canadiens spécialisés en FK. Les physiothérapeutes d’expérience étaient plus nombreux à avoir déclaré utiliser l’épreuve et l’entraînement à l’exercice que les physiothérapeutes moins expérimentés. Les études supérieures et le mentorat, particulièrement chez les cliniciens moins expérimentés, sont *Co-first authors From the: †Department of Physical Therapy, University of Toronto, Toronto, Ontario, Canada; ‡Rehabilitation Sciences Institute, University of Toronto, Toronto, Ontario, Canada; §Toronto Adult Cystic Fibrosis Centre, St. Michael’s Hospital, Unity Health Toronto, Toronto, Ontario, Canada. Correspondence to: Sarib Malik, Department of Physical Therapy, University of Toronto, 160–500 University Avenue, Toronto, Ontario M5G 1V7, Canada; [email protected]. Contributors: All authors designed the study; or collected, analyzed, or interpreted the data; and drafted or critically revised the article and approved the text. Competing Interests: None declared. Acknowledgements: The authors thank Nicole Lee Son for her assistance in participant recruitment. Copyright © Canadian Physiotherapy Association 2023. For their own personal use, users may read, download, print, search, or link to the full text. Manuscripts published in Physiotherapy Canada are copyrighted to the Canadian Physiotherapy Association. Requests for permission to reproduce this article should be made to the University of Toronto Press using the Permission Request Form: https:// www.utpjournals.press/about/permissions or by email: [email protected]. Physiotherapy Canada 2023; 75(1); 1–9; doi:10.3138/ptc-2021-0051 © Canadian Physiotherapy Association, 2023 1

2 Physiotherapy Canada, Volume 75, Number 1 recommandés pour insister sur l’importance de l’épreuve et de l’entraînement à l’exercice. Il faut corriger les obstacles au financement, au temps et à la disponibilité du personnel pour améliorer encore davantage la qualité des soins. Mots-clés: entraînement en endurance; entraînement en résistance; fibrose kystique; lacunes de la pratique professionnelle; réadaptation https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Cystic fibrosis (CF) is the most common fatal genetic of resource availability, including the lack of trained per- disease. It predominantly affects Caucasias and impacts sonnel, time, equipment, facilities, and infection control multiple body systems, including the respiratory sys- precautions.13–16 In contrast, another study found that a tems.1,2 There are over 4,370 people with CF in Canada.1 lack of equipment was not a barrier; these researchers Individuals with CF have decreased aerobic capacity2 and reported a quantity of available equipment was not being peripheral muscle strength,3 higher rates of depression used.13 Previous studies have not investigated facilita- and anxiety,4 and lower health related quality of life (QOL).1 tors, specifically, of exercises testing and training. Rather they report that the rationale, specifically, for conducting In Canada, this multisystem disease is managed by CF exercise testing and training is based on disease severity, specialized centres. In these centres, various health care in response to patients reporting decreased exercise toler- professionals with in-depth knowledge of CF and experi- ance, or conducted immediately post-discharge from acute ence in CF care provide interdisciplinary care. In general, care, and for the purpose of pre-transplant assessment.16 it is recommended that individuals with CF attend a CF It is unknown what barriers and facilitators CF centres in centre every three months; however this interval varies Canada encounter with exercise testing and training. Iden- depending on the individual's health status. The role of tifying specific barriers and facilitators within CF centres physiotherapists in CF care has evolved from mainly facil- may help strategize ways to enhance incorporating exer- itating airway clearance to incorporating different types cise testing and training in clinical practice. of exercise in assessment and treatment.5,6 The main role of physiotherapists in CF care, as outlined in the In most studies on exercise testing and training, phy- International Physiotherapy Group’s practice guidelines, sicians were the main respondents to surveys, followed are airway clearance therapy, inhalation therapy, exer- by physiotherapists and nurses.13,15 Although physicians cise testing and training, musculoskeletal physiotherapy may provide a general insight into the practice, it would management, and pre- and post- lung transplant care.5–7 be beneficial to have physiotherapists as the primary re- To our knowledge, the extent of exercise testing and train- spondents because they would have a first-hand experi- ing being performed in Canadian CF centres is unknown. ence with exercise testing and training, and would be able to provide a different perspective. Aerobic testing is defined as an assessment for an indi- vidual’s cardiopulmonary status; it is measured by max- Many entry-level health care graduates doubt their imal, submaximal, laboratory-based or field-based tests. level of competence and readiness to practise.17 It can Measures derived from aerobic testing, (e.g., Vo2max) be more challenging for them when working in a spe- are prognostic indicators for individuals with CF.8 Aero- cialized clinical area, such as CF care. Previous studies bic testing and strength testing also provide a baseline of have shown that the cognitive processes between nov- general physical health and can inform exercise prescrip- ice and expert physiotherapists differ.18–20 It is unknown tion.9 For individuals with CF, studies show that aerobic whether there is a difference in utilization of exercise training can improve pulmonary function, aerobic capac- testing and training by physiotherapists with less expe- ity, physical activity levels; ameliorate symptoms of anxi- rience relative to physiotherapists with more experience ety and depression; and enhance health related QOL.5,10,11 in CF centres. If there are discrepancies, it may highlight Strength training helps increasing force production, fos- the need to improve the learning experiences for phys- ters a lean body mass, and improves pulmonary function iotherapists in CF care to support utilization of exercise for individuals with CF.11,13 testing and training. Studies conducted in the United Kingdom, Germany, The knowledge-to-action model21 describes a process and the United States have found that general exercise by which knowledge (e.g., practice guidelines recommen- testing and training are underutilized in CF centres.13–15 dations for exercise testing and training) can be turned While these studies addressed general exercise, a study into action in clinical practice. The model involves identi- in Australia and New Zealand specifically looked at the fying a gap between knowledge and practice, and assess- extent of strength testing in CF centres and reported that ing barriers to implementating the knowledge. Following only 20% of centres included strength testing.16 These that, the model involves implementing changes, moni- results, however, cannot be generalized to Canadian CF toring and evaluating outcomes, and sustaining change. centres because of inherent differences in the health care As current physiotherapy practice regarding exercise systems. testing and training in Canadian CF centres is unknown, and in consideration of the knowledge-to-action model, Multiple studies report that a barrier to incorporating the objectives of this study were to (1) determine the exercise testing and training in clinical practice is the lack © Canadian Physiotherapy Association, 2023

Malik et al. Current Practice, Barriers to, and Facilitators of Exercise Testing and Training by Physiotherapists 3 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 utilization of aerobic testing, strength testing, aerobic the proportion of physiotherapists surveyed who perform training, and strength training in Canadian CF centres, aerobic testing, strength testing, aerobic training, and (2) identify the barriers and facilitators for implementing strength training with their CF caseload; the barriers and exercise testing and training; and (3) investigate the rela- facilitators to incorporating exercise testing and training tionship between physiotherapist’s year of clinical expe- as measured by the 5 point-Likert scale; and the demo- rience and utilization of exercise testing and training in graphics of the physiotherapists. To reduce self-report CF centres. bias and protect participant privacy, the demographic in- formation was collected in a manner that would keep the METHODS physiotherapists and CF centres anonymous. The ques- tionnaire was administered through Research Electronic Study design Data Capture (REDCap), version 7.4.1.22,23 The question- A quantitative cross-sectional web-based survey was naire piloted with physiotherapists on the cardiorespi- ratory team at St. Michael’s Hospital, modified based on administered to physiotherapists practicing in Canadian feedback, and then administered to study participants CF centres. To be eligible, participants had to be a phys- between March to April 2020. iotherapist working in one of the 42 Canadian CF centres, defined as a clinic that provides specialized interdisciplin- Statistical analysis ary care for individuals with CF and is accredited and sup- Descriptive statistics were computed, including ported financially by Cystic Fibrosis Canada. Participants were excluded if they provided only weekend and/or holi- medians, ranges and frequencies, using IBM SPSS Statis- day coverage. Ethics approval was obtained from the Uni- tics, version 26.0 (IBM Corporation, Armnok, NY). To versity of Toronto (REB 00038507). geographically present the data relating to objective 3, participants were categorized into the following groups: Recruitment (1) early career, those with <10 years of experience, (2) The secretary for the Canadian CF Physiotherapy Ad- mid career, those with >10 and <20 years of experience; and (3) late career, those with >20 years of experience. visory Group emailed all of the physiotherapists work- ing at Canadian CF centres to request their participation. RESULTS The email included a brief description of this study, an A total of 18 physiotherapists responded out of an esti- informed consent letter containing information on the purpose of the study, risks, benefits, consent, confidenti- mated 84 physiotherapists working in Canadian CF centres, ality, and publication, a link to the questionnaire including with there being between 1–3 physiotherapists per centre. an initial page to indicate consent, and the authors’ email The median years of clinical experience was 15 (range, address for questions and to request study results. Two min-max, 3–30) years, with a median full-time equivalence additional emails, spaced two weeks apart, were sent to of 0.30 (range, min-max, 0.05–1.00) hours worked/ full- remind physiotherapists to complete the questionnaire. time hours working at the CF centre. There were 67% (12) respondents from Western Canada, 17% (3) from Ontario, Data collection and 17% (3) from Quebec and Eastern Canada. Table 1 sum- The 40-item questionnaire was developed based on marizes the demographic data. previous similar studies.13–16 The questionnaire examined Table 1 Characteristics of Physiotherapists Working in CF Centres Across Canada (N = 18) Characteristic (N = 18) No. (%) of respondents % of caseload that is patients with CF 10 (56) <40% 3 (17) 40% to <80% 5 (28) 80%–100% 12 (67) Practice region 3 (17) Western Canada (BC/AB/SK/MB) 3 (17) Ontario Quebec and Eastern Canada (NB/NS/NL) 4 (22) 14 (78) Clinical practice setting Outpatient only 12 (67) Inpatient and outpatient 6 (33) Clinical practice population Paediatric only Adult and paediatric CF = cystic fibrosis; BC = British Columbia; AB = Alberta; SK = Saskatchewan; MB = Manitoba; NB = New Brunswick; NS = Nova Scotia; NL = Newfoundland and Labrador. © Canadian Physiotherapy Association, 2023

4 Physiotherapy Canada, Volume 75, Number 1 Table 2 Implementation of Aerobic and Strength Testing, and Aerobic and Strength Training in CF Centres in Canada No. of PTs who implement Proportion of CF caseload for whom testing/training is implemented* (N = 18) https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Type of testing or training Small† Medium† Large† Aerobic testing 8 71 – Strength testing 7 7– – Aerobic training 14 61 7 Strength training 12 91 2 Aerobic testing and training 7 Strength testing and training 6 * Of physiotherapists who implement testing/training. † Small = 0 to <40% of CF caseload; medium = 40% to <60% of CF caseload; large = 60–100% of CF caseload. CF = cystic fibrosis; PT = physiotherapist. Utilization of exercise testing and training reported sometimes (50% of the time) referring out for Table 2 summarizes utilization of exercise testing and strength training. All but one of the respondents who pre- scribed aerobic or strength training reported encouraging training: 44% (8) administered aerobic testing, 39% (7) participation in recreational sports and fitness classes. administered strength testing, 78% (14) prescribed aerobic training, and 67% (12) prescribed strength training. Addi- Rationale for, facilitators of, and barriers to exercise testing and tionally, 39% (7) administered both aerobic testing and training aerobic training, and 33% (6) administered both strength testing and training. Tables 3, 4 and 5 summarize the rationale for, facilita- tors of, and barriers to exercise testing and training. The Among those who administer aerobic testing, 88% (7 most commonly reported reason for performing aero- out of 8) use the six minute walk test, 25% (2 out of 8) use bic testing was to establish baseline values for patients, the incremental shuttle walk test, and 13% (1 out of 8) 88% (7 out of 8); followed by establishing eligibility for utilized the Bruce protocol. Annual aerobic testing was transplant, 75% (6 out of 8); responding to the request of reported by 75% (6 out of 8). For aerobic training, 92% physicians/nurse practitioners, 75% (6 out of 8); inform- (13 out of 14) of respondents recommended that their pa- ing exercise prescription, 50% (4 out of 5); and estimat- tients engage in aerobic training more than three times ing functional independence, 50% (4 out of 8). Of those per week. Comparatively, 58% (7 out of 12) of respondents who perform strength testing, their rationale included recommended that strength training to be performed informing exercise prescription 86% (6 out of 7); estab- three to four times per week. With respect to prescrib- lishing baseline values for patients 71% (5 out of 7); and ing an aerobic home exercise programme, 71% (10 out of estimating functional independence 71% (5 out of 7). 14) respondents reported prescribing such a programme No participants reported aerobic or strength testing as more than 50% of the time. In contrast, 58% (7 out of 12) requirements by their place of work. respondents reported prescribing a strength-based home exercise programme less than 25% of the time. Regarding The most frequently reported facilitator for aerobic referring to other health care professionals for exercise testing and strength testing was sufficient infection con- training, 86% (12 out of 14) of respondents reported never trol, 72% (13 out of 18). The most frequently reported or rarely (0%–25% of the time) referring out for aerobic facilitator for aerobic and strength training was the phys- training, while 67% (8 out of 12) of respondents reported iotherapist having sufficient knowledge to prescribe train- never or rarely (0%–25% of the time) referring out for ing programmes, 72% (13 out of 18) and 61% (11 out of 18), strength training, and 25% (3 out of 12) of respondents respectively. Table 3 Rationale for the Administration of Aerobic Testing and Strength Testing Utilized by Physiotherapists Working in CF Centres in Canada Aerobic testing, % (n = 8) Strength testing, % (n = 7) Establishing baseline values 88 72 Informing exercise prescription 50 86 Estimating functional independence 50 71 Requested by physician/nurse practitioner 75 14 Establishing eligibility for transplant 75 N/A Note: Participants could select one or more response(s). CF = cystic fibrosis. © Canadian Physiotherapy Association, 2023

Malik et al. Current Practice, Barriers to, and Facilitators of Exercise Testing and Training by Physiotherapists 5 Table 4 Facilitators for the Implementation of Aerobic and Strength Testing, Aerobic and Strength Training as Determined by Physiotherapists Working in CF Centres in Canada https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Aerobic testing, % Strength testing, % Aerobic training, % Strength training, % Sufficient infection control 72 72 67 56 Sufficient knowledge 44 61 72 61 Sufficient equipment 44 33 50 44 Patient(s) willing to participate 39 33 17 11 Sufficient staff availability 22 22 33 22 Sufficient time 17 22 17 17 Sufficient funding 6 6 6 17 Note: Participants could select one or more response(s). CF = cystic fibrosis. Table 5 Barriers to the Implementation of Aerobic and Strength Testing, and Aerobic and Strength Training as Determined by Physiotherapists Working in CF Centres in Canada Aerobic testing, % Strength testing, % Aerobic training, % Strength training, % Insufficient funding 67 61 56 61 Insufficient time 61 61 50 61 Insufficient staff availability 56 56 56 56 Insufficient equipment 39 45 28 28 Patient(s) unwilling to participate 17 17 11 17 Insufficient infection control 6 6 11 22 Insufficient knowledge 17 11 – 6 Note: Participants could select one or more response(s). CF = cystic fibrosis. Among the participants, 67% (12) reported insufficient by physiotherapists at Canadian CF centres. The main funding as the primary barrier to administering aerobic findings were that aerobic testing, strength testing, aerobic testing; 56% (10) reported insufficient funding and staff training and strength training are underutilized, with aer- availability as the main barriers to the implementing aer- obic training being the most utilized. The most frequently obic training; 61% (11) reported insufficient funding and reported barriers to exercise testing and training were in- time as main barriers to strength testing and strength sufficient funding, time, and staff availability. The most training. frequently reported facilitators were physiotherapists hav- ing appropriate knowledge to perform testing and train- Years of experience and utilization of exercise testing and ing, and sufficient infection control practices. Mid- and training late-career physiotherapists tend to utilize exercise testing and training more than their early-career colleagues. Figure 1 depicts the utilization of exercise testing and training among physiotherapists based on their years of The results of our study regarding the utilization of experience in CF care. Of the early-career group, 33% (2 exercise testing and training were aligned with previous out of 6) of physiotherapists reported performing aero- studies conducted in the United Kingdom, Germany, and bic testing, strength testing, and strength training, while the United States.13–15 The UK study also demonstrated aerobic training was reported by 67% (4 out of 6). In the that aerobic training was more commonly utilized than mid-career group, aerobic testing was reported by 50% (4 aerobic testing,15 which is similar to our study results. The out of 8), strength testing by 25% (2 out of 8), and aerobic previously mentioned studies focused solely on aerobic and strength training by 75% (6 out of 8). For the late-ca- testing and aerobic training. In contrast, the study in Aus- reer group, aerobic testing was reported by 50% (2 out of tralia and New Zealand is uniquely similar to ours in that 4), strength testing by 75% (3 out of 4). All of the late-ca- it looked at strength testing in addition to aerobic testing. reer physiotherapists reported prescribing aerobic and That study reported a higher utilization of aerobic testing strength training to their patients in the last 12 months. than our study, but similar preferential use of field-based exercise tests over lab-based tests, and similar underutili- DISCUSSION zation of strength testing.16 In this study, we investigated the current practice of, We postulate that the underutilization of strength test- barriers to, and facilitators of, exercise testing and training ing and training may be due to CF care historically focusing © Canadian Physiotherapy Association, 2023

6 Physiotherapy Canada, Volume 75, Number 1 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 100 Strength tes ng Aerobic training Strength training Propor on of respondents 90 80 70 60 50 40 30 20 10 0 Aerobic tes ng Early career Mid career Late career Figure 1 Proportion of respondents implementing exercise testing and training by category (aerobic testing, strength testing, aerobic training, and strength training). Note: Early career (≤10 years experience) n = 6, mid career (>10 years and <20 years of experience) n = 8, late career (≥20 years experience) n = 4. on managing respiratory function. However, there has the questionnaire. Further, standardized aerobic testing been a recent increase in focus on muscle impairments is important for determining exercise capacity, symptoms in people with CF. In particular, a study found that altered related to exercise, the need for oxygen supplementa- expression of the CF transmembrane conductance regu- tion, and to monitor the efficacy of a training programme, lator (CFTR) gene in skeletal muscle results in disruption all crucial for aerobic exercise prescription according to of cell electrochemical gradients, which may impact the best practice guidelines.6 Additionally, due to COVID-19, excitation-coupling necessary for skeletal muscle func- many patients may be exercising independently, without tion.24 On a macroscopic level, individuals with CF have medical supervision. This further emphasizes the need small thigh muscles and diminished hand grip strength.25 for initial exercise testing as a basis for safe exercise pre- Given these physiological impairments, there is a need scription, especially for patients with a history of adverse to optimize functional strength testing and prescribe effects during exercise. There appears to be a lack of aero- strength training to ameliorate these impairments. It is bic testing performed by physiotherapists at Canadian CF estimated to take 17 years for research to translate into centres, and while understandable considering barriers practice,26 which may help explain the underutilization of (e.g., insufficient funding, time, and staff availability) it is strength testing and training. As the average lifespan of a significant issue that should be addressed. individuals with CF lengthens due to advances in health care, such as a new class of drugs, CFTR modulator thera- One of our objectives was to investigate facilitators for pies, that modulate the function of CFTR proteins that are exercise testing and training. Within this objective, we defective due to mutations the CFTR gene, musculoskel- further investigated the clinicians’ rationales for imple- etal issues will become more prominent, resulting in an menting exercise testing. Our study found that the most increased need for exercise, such as strength training, to frequently reported facilitators for exercise testing and improve physical functioning and QOL.12 training are sufficient infection control practices, and physiotherapists possessing adequate knowledge for test- Our study found aerobic testing to be less utilized ing protocols. Infection control practices are essential to than aerobic training. This raises the question of what minimize patient-to-patient spread of pathogens, which background information physiotherapists use to pre- is crucial for individuals with CF at all times. The rationale scribe aerobic training. It is plausible that other health for performing testing procedures was to establish base- care professionals (e.g., respiratory therapists) conduct line values of patients and guide exercise prescription. the exercise testing, and that physiotherapists conduct Similarly, the study in Australia and New Zealand, which informal exercise testing (e.g., observing patients’ mobil- discussed only the rationale for exercise testing, reported ity) and then prescribe exercise training. Or, exercise may that it is conducted for patient annual assessments and in be prescribed within the general parameters of intensity response to reduced exercise tolerance.16 by using the Borg Dyspnea Scale or a range of predicted heart rates. However, our participants did not indicate the With respect to the barriers for exercise testing and above alternative methods to inform exercise training in training, our study had similar findings to research conducted in the United Kingdom, and Australia and © Canadian Physiotherapy Association, 2023

Malik et al. Current Practice, Barriers to, and Facilitators of Exercise Testing and Training by Physiotherapists 7 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 New Zealand; that is, the most common barriers that such as CF centres, and the value it would provide less hinder the utilization of exercise testing and training are experienced physiotherapists in developing their skills. insufficient funding, time, and staff availability at CF cen- Further, online resources tailored towards enhancing tres.15,16 A possible explanation for the commonalities in practice of novice CF physiotherapists such as Australia’s barriers that CF physiotherapists in the United Kingdom, CFphysio.com, may be a good supplement to mentorship Australia and New Zealand, and Canada,15,16 encounter sessions. Many workplaces also offer educational grants may be that they all have universal, publicly funded health that may incentivize physiotherapists to further their pro- care systems. Thus, barriers such as insufficient funding fessional development. must be examined at a health systems level as opposed to studying individual CF centres. This study investigated the physiotherapy practices in CF Centres prior to the COVID-19 pandemic; however, it It is widely acknowledged that the health care systems is imperative to highlight the impact of the pandemic on in many Canadian provinces struggle to procure suffi- current and future practice. As many in-person services cient funding.-27,28 Previous Canadian research highlights were disrupted, physiotherapists modified their practice the costs associated with hospitalization of individuals by incorporating telerehabilitation. While the efficacy of with CF, citing an average of $21,000 per hospitalization telerehabilitation during the pandemic is still being inves- in 2014 for pulmonary exacerbation.29 Research has also tigated, a previous study investigating the remote admin- shown that individuals who undertake aerobic training istration of exercise training for individuals with chronic have lower risks of hospitalization due to their higher aer- lung conditions concluded that individuals receiving su- obic fitness.30 Taken together, it is imperative that phys- pervised remote aerobic training demonstrated improve- iotherapists working in Canadian CF centres advocate ments in endurance exercise capacity as measured by for additional funding for exercise testing and training to increased shuttle walk test times.34 This needs to be con- help mitigate hospitalization costs but more importantly, firmed with the CF population. The COVID-19 pandemic to improve patient outcomes. and subsequent research of efficacy of practice during that time may provide a unique opportunity to expand Our study reports that a substantially higher propor- CF care, including exercise testing and training, to virtual tion of experienced physiotherapists, those with greater platforms, making CF care more accessible to Canadians than 10 years of experience, perform exercise testing and who live far from a CF centre. training compared to their less experienced colleagues. To our knowledge, there are no previous studies examining Based on the knowledge-to-action model created by Gra- the association between physiotherapists’ clinical expe- ham and colleagues, our study identified a knowledge-prac- rience and utilization of exercise testing and training in tice gap between practice guidelines’ recommendations for their CF practice in Canada. However, clinical experience exercise testing and training and its clinical utilization, and has been previously shown to be related with clinical deci- barriers and facilitators to utiliza- tion.21 To overcome the sion-making. Novice clinicians tend to prioritize their aca- gap between practice guidelines and clinical practice, we demic knowledge, while experienced clinicians transition propose the following recommendations. towards using their clinical experience when making clin- ical decisions.20 Studies show that physiotherapists with We recommend education regarding the importance less clinical experience prefer to seek assistance when and benefits of aerobic testing, strength testing, aerobic making clinical decisions, as they report less self-efficacy training and strength training in CF care. More specifically, and confidence in their decisions.19,20 Additionally, another with regards to early-career physiotherapists, literature study noted that experienced physiotherapists were more supports continued educational opportunities and men- confident in managing uncertainty during decision-mak- torship to increase confidence and skills, which translates ing and felt they could balance risks and benefits in their into improved decision-making in clinical practice. practice.31 Less experienced physiotherapists also demon- strated having lower confidence with assessment and Additionally, we recommend increased funding and treatment.32 When taken together, a lack of clinical expe- staffing to minimize the barriers that physiotherapists rience and confidence may translate into less experienced encounter utilizing exercise testing and training. Future physiotherapists underutilizing exercise testing and train- studies may investigate how increased funding can be ing in their practice; however, this requires further inves- allocated to best enable increased exercise testing and tigation to confirm. Wainwright and colleagues noted that training. both novice and experienced physiotherapists working in neurologic physiotherapy valued mentorship in develop- A limitation of our study is that other health care pro- ing clinical decision-making.20 Furthermore, students and fessionals may have conducted exercise testing or train- novice physiotherapists felt that learning from peers was ing with the patients of physiotherapists responding to essential when developing clinical skills.33 This highlights our study, which was not reflected in our questionnaire. the benefits of mentorship in specialized practice areas, However, we specifically directed our study towards phys- iotherapists working at CF centres to elucidate their cur- rent practice. We had a smaller sample size than expected, which may have been due to the following: the timeframe © Canadian Physiotherapy Association, 2023

8 Physiotherapy Canada, Volume 75, Number 1 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 for data collection was reduced due to data collection on the importance of exercise testing and training in CF occurring during the COVID-19 pandemic. Also physio- care, and that the barriers to exercise testing and training therapists may have been focused on their clinical work be addressed to enable improved quality of care and out- secondary to changes in personal protective equipment comes for individuals with CF. policy, redeployment, and prioritizing patients; therefore, had less opportunity to respond to our questionnaire. REFERENCES Furthermore, a large proportion of our respondents 1. Cystic Fibrosis Canada. The Canadian Cystic Fibrosis Registry: 2017 were from Western Canada, limiting the generalizability annual data report [Internet]. Cystic Fibrosis Canada; 2018 Dec [cited of our findings to physiotherapist practice across all Ca- 2020 May 18]. Available from: https://www.cysticfibrosis.ca/uploads/ nadian CF centres. Another limitation is that we do not Registry%20Report%202017/2017%20Registry%20Annual%20 know how many of Canada’s 42 CF centres represented in Data%20Report.pdf the response. This is because we ensured complete ano- nymity of all respondents, including which CF centres 2. Troosters T, Langer D, Vrijsen B, et al. Skeletal muscle weakness, they worked at, to reduce response bias. exercise tolerance and physical activity in adults with cystic fibrosis. Eur Respir J. 2009 Jan;33(1):99–106. As our study did not examine the specific testing and training protocols used at Canadian CF centres, future 3. Elkin SL, Williams L, Moore M, et al. Relationship of skeletal muscle studies should investigate the protocols used. This may mass, muscle strength and bone mineral density in adults with cystic help inform a future Canadian best practice guideline that fibrosis. Cyst Fibros. 2000;6. CF centres could follow to standardize the high level of care they provide. Future studies should also continue the 4. Quittner AL, Goldbeck L, Abbott J, et al. Prevalence of depression and application of the knowledge-to-practice model through anxiety in patients with cystic fibrosis and parent caregivers: results its subsequent stages of monitoring the change in utili- of The International Depression Epidemiological Study across nine zation of exercise testing and training, evaluating patient countries. Thorax. 2014 Dec;69(12):1090–7. outcomes, and ensuring sustainability of increased exer- cise testing and training in CF centres. 5. Button BM, Wilson C, Dentice R, et al. Physiotherapy for cystic fibrosis in Australia and New Zealand: A clinical practice guideline. CONCLUSION Respirol Carlton Vic. 2016 May;21(4):656–67. Aerobic testing, strength testing, aerobic training and 6. Morrison L, Parrott H. Standards of care and good clinical practice strength training are underutilized at Canadian CF cen- for the physiotherapy management of cystic fibrosis [on the tres. Insufficient funding, time, and staff availability are internet]. Cystic Fibrosis Trust; 2020 Nov [cited 2022 Sept 18] the most reported barriers to the implementation of exer- Available from: https://www.cysticfibrosis.org.uk/the-work-we-do/ cise testing and training. Additionally, a greater propor- resources-for-cf-professionals/consensus-documents tion of physiotherapists with more clinical experience in CF care tend to implement exercise testing and training. 7. International Physiotherapy Group for Cystic Fibrosis. Physiotherapy We recommend that the barriers of time and funding be for People with Cystic Fibrosis: from Infant to Adult. 7th ed. 2019 addressed; physiotherapists continue to learn about the [cited 2022 Sept 20]. Available from: https://www.ecfs.eu/sites/ importance of testing and training for people with CF; default/files/general-content-files/working-groups/IPG%20CF_ and physiotherapists support one another, especially ear- Blue%20Booklet_7th%20edition%202019.pdf ly-career clinicians, to increase the utilization of exercise testing and training in CF care. 8. Urquhart DS, Saynor ZL. Exercise testing in cystic fibrosis: Who and why? Paediatr Respir Rev. 2018 Jun;27:28–32. KEY MESSAGES 9. Martin C, Chapron J, Hubert D, et al. Prognostic value of six What is already known on this topic minute walk test in cystic fibrosis adults. Respir Med. 2013 To improve patient outcomes, exercise testing and Dec;107(12):1881–7. training are an important aspect of the physiotherapists’ 10. 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Clinician’s Commentary on Malik et al.1 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Cystic fibrosis (CF) is a multisystem disease impacting and the effect on physical fitness and physical activity are organs beyond the lungs, including the pancreas, gastro- unclear,6 these drugs result in demonstrated improve- intestinal tract, liver, sweat glands, reproductive organs, ments in lung function, symptoms, and respiratory exac- and skeletal muscle.2,3 Advances in CF therapy, includ- erbations. This may provide a rationale and opportunity ing inhaled antibiotics, mucolytic therapies, nutritional to emphasize musculoskeletal fitness through exer- support, lung transplantation, and most recently CF cise counselling, testing, and training in people with an transmembrane conductance regulator (CFTR) modula- increased respiratory capacity to encourage participation tor drugs have increased the median age of survival for in exercise, address the CFTR modulator side effect of Canadians with CF from 31.9 years in 1990 to 55.4 years weight gain, promote a healthy body composition, and in 2020.4,5 This shift towards more adults ageing with CF impact some of the effects of ageing on physical health. will potentially be accompanied by the presence of vari- In addition, the improvement in respiratory function and ous cardiometabolic and musculoskeletal comorbidities symptoms may allow deferral of lung transplantation, in people with CF. resulting in older lung transplant patients with CF. Bet- ter management of extrapulmonary comorbidities could In Canada, CF is managed by specialized interdisci- mitigate the negative effect on pre- and post-transplant plinary paediatric and adult centres, and in 2020 there outcomes. were more than 18,000 CF clinic visits.5 Malik and col- leagues administered an online survey to examine cur- The most frequently reported facilitator for aerobic rent physiotherapy practices, barriers, or facilitators of and strength testing in this study was sufficient infection these CF centres in regard to exercise testing and train- control. During the COVID-19 pandemic there has been ing.1 Both aerobic and resistance testing and training a shift from in-patient to out-patient CF care,5 as well as were underutilized, which aligns with previous findings to tele-rehabilitation or hybrid rehabilitation models for at other international CF centres. chronic lung disease populations. Although there are reported limitations with remote functional assessments,7 Understanding the rationale for exercise testing and remote monitoring technology and tools to assess and training in the care of CF patients is important. A clear monitor vital signs and activity metrics present an alterna- use case is people with end-stage respiratory disease who tive option for tracking disease and functional trajectories undergo routine exercise assessment for several reasons ahead of or between scheduled CF clinic appointments. including supplemental oxygen prescription, determin- ing lung transplant eligibility, and monitoring exercise The most frequently reported facilitator for aerobic training and exercise capacity during pre-habilitation, and strength training in this study was sufficient knowl- and early post-operative rehabilitation. The rationale for edge to prescribe training programmes. This is an area exercise assessment and training in non-transplant pop- that could be further optimized as currently there is lim- ulations to establish a baseline functional level, track the ited evidence for CF-specific exercise from studies with efficacy of medical and rehabilitative therapies, and pre- low to moderate methodological quality and a lack of scribe exercise may vary. widely accepted physical activity guidelines specifically targeted to CF. Furthermore, the effect of CFTR modulator Recently Gruet and colleagues advocated for rethink- therapies on exercise is in the early phases.6,8 ing exercise in CF, specifically in regard to adapting train- ing concepts and strategies to an ageing CF population A third objective of this study was to investigate the with associated comorbidities.6 While treatment for the relationship between the physiotherapist’s years of clin- paediatric CF population focuses on the development ical experience, and utilization of exercise testing and of motor skills and neuromuscular fitness to normalize training in a specialized CF practice. Experienced phys- physical activity participation from a young age and at an iotherapists reported greater utilization of exercise test- early stage of CF, adults with CF require approaches that ing and training in practice. Formal academic training will facilitate long-term maintenance of habitual phys- programmes and post-graduate education highlight the ical activity and exercise, particularly in the new era of physiological importance of and clinical skills for exercise disease-modifying CFTR modulator therapies. Although testing and training, but competencies for evaluating the the long-term impact of CFTR modulators are not known emerging literature on new medical management and © Canadian Physiotherapy Association, 2023. For their own personal use, users may read, download, print, search, or link to the full text. Manuscripts published in Physiotherapy Canada are copyrighted to the Canadian Physiotherapy Association. Requests for permission to reproduce this article should be made to the University of Toronto Press using the Permission Request Form: https:// www.utpjournals.press/about/permissions or by email: [email protected]. Physiotherapy Canada 2023; 75(1); 10–11; doi:10.3138/ptc-2021-0051-cc 10 © Canadian Physiotherapy Association, 2023

Clinician’s Commentary on Malik et al. 11 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 incorporating new knowledge are essential for clinicians fibrosis specialized centres in Canada. Physiother Can. 2023; 75(1): 1–9. at all stages of their career. https://doi.org/10.3138/ptc-2021-0051. 2. Ode KL, Chan CL, Granandos A, et al. Endocrine complications Cystic fibrosis is a multisystem disease that, over of cystic fibrosis: a multisystem disease of the endocrine organs. the past few decades, has been evolving in clinical pre- Semin Respir Crit Care Med. 2019;40:810–24. https://doi. sentation and lifespan due to changes in medical man- org/10.1055/s-0039-1697917. Medline:31679155 agement. Physiotherapy practice needs to continue to 3. Wu K, Mendes PL, Sykes J, et al. Limb muscle size and contractile evolve alongside these medical advances as an increased function in adults with cystic fibrosis: a systematic review and meta- emphasis on exercise and physical activity may address analysis. J Cyst Fibros. 2021;20:e53–62. https://doi.org/10.1016/j. some of the emerging issues with shifting demograph- jcf.2021.02.010. Medline:33648899 ics and the benefits and side effects of disease-modify- 4. Stephenson AL, Tom M, Berthiaume Y, et al. A contemporary survival ing therapies. Leveraging technology and incorporating analysis of individuals with cystic fibrosis: a cohort study. Eur Respir innovative methods of assessing, monitoring, and train- J. 2015;45:670–9. https://doi.org/10.1183/09031936.00119714. ing remotely should be considered in this modern era of Medline:25395034 CF care. Clinical rehabilitation research will continue to 5. Cystic Fibrosis Canada. The Canadian cystic fibrosis registry 2020 play an important part of this transition to strengthen the annual data report. Cystic Fibrosis Canada; 2022. Accessed evidence base and inform clinical practice guidelines. September 4, 2022. https://www.cysticfibrosis.ca/ registry/2020AnnualDataReport.pdf. Lisa Wickerson PT, PhD 6. Gruet M, Saynor ZL, Urquhart D, et al. Rethinking physical exercise Assistant Professor, Department of Physical Therapy, training in the modern era of cystic fibrosis: a step towards optimising short-term efficacy and long-term engagement. J Cyst University of Toronto; Affiliate Scientist, TGHRI & Fibros. 2022;21:e83–98. https://doi.org/10.1016/j.jcf.2021.08.004. Ajmera Transplant Centre, University Health Medline:34493444 Network, Toronto, Ontario, Canada; 7. Holland AE, Malaguti C, Hoffman M, et al. Home-based or remote [email protected]. exercise testing in chronic respiratory disease, during the COVID-19 pandemic and beyond: a rapid review. Chron Respir Dis. 2020;17: REFERENCES 1479973120952418. https://doi.org/10.1177/1479973120952418. Medline:32840385 1. Malik S, Levi B, Chan A, et al. Current practice, barriers to, and 8. Radtke T, Nolan SJ, Hebestreit H, et al. Physical exercise training facilitators of exercise testing and training by physiotherapists in cystic for cystic fibrosis. Cochrane Database Syst Rev. 2015;28:CD002768. https://doi.org/10.1002/14651858.cd002768.pub3. Medline:26116828 © Canadian Physiotherapy Association, 2023

https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 ORIGINAL RESEARCH Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors: A Systematic Review and Meta-Analysis Priyanshi S. Akbari, BSc, MScPT; Yusra Hassan, BSc, MScPT; Lisa Archibald, BSc, MScPT; Tania Tajik, BSc, MScPT; Kaitlin Dunn, BSc, MScPT; Mara Berris, BSc, MScPT; Jenna Smith-Turchyn, MscPT, PhD ABSTRACT Purpose: To determine if cancer survivors who perform physical activity (PA) during chemotherapy have improved levels of cognitive function compared to those who do not. Method: E-databases (Ovid MEDLINE, Embase, CINAHL, PsycINFO, AMED) were searched from inception to February 4, 2020. Quantitative studies that assessed cognitive outcomes for adults with any cancer type who received chemotherapy concurrent with PA were selected. Risk of bias was assessed using Cochrane’s RoB 2, ROBINS-I, and Newcastle-Ottawa scales. A meta-analysis was performed using standardized mean difference (SMD). Results: Twenty-two studies (15 randomized controlled trials [RCTs] and 7 non-RCTs) met the inclusion criteria. The meta-analysis demonstrated that combined resistance and aerobic training had a small yet statistically significant effect on social cognition compared to usual care (SMD 0.23 [95% CI: 0.04, 0.42], p = 0.020). Conclusions: Combined resistance and aerobic exercise may benefit social cognition in cancer survivors undergoing chemotherapy. Due to high risk of bias and low quality of evidence of included studies, we recommend further investigation to support these findings and make specific PA recommendations. Key Words: cancer; chemotherapy; cognition; physical activity; physical therapy. RÉSUMÉ Objectif : déterminer si les survivants du cancer qui font de l’activité physique (AP) pendant la chimiothérapie ont une meilleure fonction cognitive que ceux qui n’en font pas. Méthodologie : les chercheurs ont fouillé des bases de données électroniques (Ovid MEDLINE, Embase, CINAHL, PsycINFO, AMED) à compter de leur création jusqu’au 4 avril 2020. Ils ont sélectionné les études quantitatives qui évaluaient les issues cognitives des adultes atteints de quelque type de cancer que ce soit et qui avaient été sous chimiothérapie tout en faisant de l’AP. Ils ont évalué le risque de biais au moyen des échelles RoB 2 et ROBINS-I de Cochrane et de l’échelle de Newcastle-Ottawa et ont effectué une méta-analyse au moyen de la différence moyenne standardisée (DMS). Résultats : au total, 22 études (15 essais cliniques randomisés [ÉCR] et sept essais cliniques non randomisés [non-ÉCR]) respectaient les critères d’inclusion. La méta-analyse a démontré que la combinaison d’exercices de résistance et d’exercices aérobiques avait un effet statistique petit, mais significatif, sur la cognition sociale par rapport aux soins habituels (DMS = 0,23 [IC a 95 % : 0,04, 0,42], p = 0,020). Conclusions : la combinaison d’exercices de résistance et d’exercices aérobiques peut être bénéfique à la cognition sociale des survivants du cancer sous chimiothérapie. Étant donné le risque élevé de biais et la faible qualité des données probantes des études retenues, les chercheurs recommandent de poursuivre les recherches pour appuyer ces résultats et faire des recommandations particulières en matière d’AP. Mots-clés : activité physique; cancer; chimiothérapie; cognition; physiothérapie Approximately 225,800 new cases of cancer and 83,300 deficits in memory, processing speed, concentration, and deaths from cancer occurred in Canada in 2020.1 Nega- multi-tasking.2,3 Cognition is defined as mental processes tive cognitive effects occur in 75% of survivors undergo- that are related to the acquisition, storage, manipula- ing chemotherapy with common impairments including tion, and retrieval of information.4 Various domains of From the School of Rehabilitation Science, McMaster University, Hamilton, Ontario, Canada. Correspondence to: Jenna Smith-Turchyn, School of Rehabilitation Science, Faculty of Health Sciences, McMaster University, 1400 Main Street West, Institute for Applied Health Sciences (IAHS) Building, Room 403, Hamilton, Ontario L8S 1C7, Canada; [email protected]. Contributors: All authors designed the study, collected, analyzed, or interpreted the data; and drafted or revised the article and approved the final draft. Competing Interests: None declared. © Canadian Physiotherapy Association, 2023. For their own personal use, users may read, download, print, search, or link to the full text. Manuscripts published in Physiotherapy Canada are copyrighted to the Canadian Physiotherapy Association. Requests for permission to reproduce this article should be made to the University of Toronto Press using the Permission Request Form: https:// www.utpjournals.press/about/permissions or by email: [email protected]. Physiotherapy Canada 2023; 75(1); 12–21; doi:10.3138/ptc-2021-0032 12 © Canadian Physiotherapy Association, 2023

Akbari et al. Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors 13 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Figure 1 Domains of cognition and underlying processes. Adapted from Cambridge Cognition (© Copyright 2018 Cambridge Cognition Limited. All rights reserved).4 cognition exist, including social cognition, executive func- understanding regarding the effectiveness of PA relative to tion, memory, attention, and psychomotor speed, which the timing of treatment.6.9 Specifically, a gap exists regard- work together to optimize mental functioning (Figure 1).4 ing the evidence on the cognitive impact of PA during che- motherapy. The purpose of this systematic review (SR) and Physical activity (PA) is an umbrella term that encom- meta-analysis (MA) is to determine if cancer survivors who passes any active body movement that requires energy perform PA during chemotherapy have improved levels of expenditure.5 PA includes unstructured activities, such cognitive function compared to those who do not. as household chores, work duties, and sports, and struc- tured activities such as exercise.12 Exercise and PA are easily METHODS accessible interventions that have been shown to alleviate This SR was developed according to the Preferred side effects of chemotherapy and produce positive health outcomes.6–8 Additionally, a systematic review (SR) of epi- Reporting Items for Systematic Reviews and Meta-Analyses demiological studies demonstrated that PA performed (PRISMA) and Cochrane Handbook recommendations.11,12 before, during, or after cancer diagnosis has a strong A protocol was developed prior to conducting this review association with reduced all-cause and cancer-specific and has been registered in the PROSPERO database (reg- mortality.9 Based on these findings, the American College istration number: CRD42020171191). of Sports Medicine and Cancer Care Ontario developed exercise recommendations for cancer survivors, which Inclusion criteria suggests that moderate intensity exercise during active Studies selected in this SR included adults (> 18 years) treatment is safe and beneficial.7–8 Recent evidence found acute and chronic ameliorative effects of PA on cancer-re- diagnosed with any type of cancer who were receiving lated cognitive impairments.6,9 Acutely, increased vascular- chemotherapy at the time of intervention, used a PA inter- ization, central nervous system blood flow, and hormone vention, performed evaluation of cognitive outcomes, production beneficial for neural structure and function, and had a quantitative study design of any form. and decreased pro-inflammatory cytokines and oxidative stress play a role in relieving cognitive symptoms after exer- To meet the eligibility criteria of performing evaluation cise.10 Chronically, exercise increases anti-inflammatory of a cognitive outcome, outcome measures had to meet neurotransmitters like dopamine, leading to improved one of the classifications of the Cambridge Cognition executive function and synaptic plasticity.6,9,10 domains of cognition.4 Interventions that met our inclu- sion criteria could involve any form of PA. Currently, a growing body of evidence exists exploring the cognitive effects of PA in survivors at various time points Exclusion criteria during the cancer trajectory.5,8 However, there is limited Articles were excluded if they were not written in English, were protocols only, included an animal population only, © Canadian Physiotherapy Association, 2023

14 Physiotherapy Canada, Volume 75, Number 1 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 included children only (populations < 18 years of age), or were summarized using a narrative synthesis. No addi- included populations not receiving chemotherapy concur- tional analyses were conducted. rently with the PA intervention. The GRADE approach was implemented to assess the Search methods quality of the evidence for all unique outcomes related to Reviewers searched for published work from incep- cognition.12 This approach assesses risk of bias, inconsis- tency, indirectness, imprecision, and the risk of publica- tion to February 4th, 2020. The five electronic databases tion bias across each outcome.12 GRADEpro was used to searched were Ovid MEDLINE (1946 to current), Embase generate Summary of Findings (SoF) and Evidence Profile (1974 to current), CINAHL (1961 to current), PsycINFO (EP) tables (online Appendices 3, 4, and 5).14 (1806 to current), and AMED (1985 to current). Assessing risk of bias within and across studies Within each database, search terms for cancer, PA, and Full-text articles were assessed for risk of bias in dupli- cognitive function were included. See online Appendix 1 for the search strategy. Reference lists of recent reviews cate by three reviewers (PSA, LA, YH). Assessors were and trials were scanned to ensure no additional refer- blinded to the author, year, journal, and title. For assess- ences met the inclusion criteria. ing bias in RCTs, the Cochrane Risk of Bias in Random- ized Trials (RoB 2.0) tool was used.15 For non-RCTs, the Data collection Risk of Bias in Non-randomized Studies of Interventions (ROBINS-I) tool was used.16 As a deviation from the pro- Study screening and selection tocol, the Newcastle-Ottawa Scale (NOS) was added to All studies identified through the electronic database assess studies of single group designs because this tool allowed for increased accuracy in investigating bias for search were uploaded to Covidence, a literature manage- this study type.17 Across all tools, inter-rater agreement ment software system.13 Titles and abstracts were screened was assessed and reported using Cohen’s Kappa coeffi- in duplicate by three reviewers (MB, KD, TT) using the cient. Studies were not excluded from this SR based on inclusion criteria. The first ten titles and abstracts were their rated risk of bias. Risk of bias assessments were used screened by all three reviewers to ensure consistency in to inform the GRADE SoF and EP tables to assess the over- decision-making. Titles and abstracts deemed to meet all all quality of evidence presented in this SR. Across stud- criteria by at least one reviewer continued onto full-text ies, risk of bias was assessed per outcome, as shown in the screening. All full-text screening was completed in dupli- SoF and EP tables (online Appendices 3, 4, and 5). cate. Studies were included when both reviewers accepted the article. Disagreements were resolved through discus- Assessment of heterogeneity sion with a third reviewer (JST). See online Appendix 2 for Heterogeneity between study effect measures in the excluded studies and reasoning. MA was assessed using both the 2 test and the I2 statis- Data extraction tic. As outlined by the Cochrane Handbook, for the 2 test, Three reviewers (PSA, LA, YH) were blinded to the a P value less than 0.10 indicated statistically significant heterogeneity.12 I2 measured the proportion of results review authors prior to performing full-text data extraction affected by heterogeneity compared to chance. I2 cutoffs in duplicate. Disagreements were resolved through con- were used based on the Cochrane Handbook recommen- sulting a third reviewer to reach consensus. Authors were dations, where 0%–40% indicated low heterogeneity.12 contacted by email for missing data if required for anal- yses (e.g., means, standard deviations). If authors were RESULTS unreachable, the research was only included narratively. Study selection Critical appraisal and synthesis Through database searching, 8,841 studies were iden- Data synthesis tified for title and abstract screening; 108 studies met the A random-effects MA model for continuous data was inclusion criteria and were reviewed in full-text screening. Twenty-two studies met inclusion criteria.18–39 Five of the completed due to the likelihood of heterogeneity between selected 22 studies were analyzed through a MA.18–22 The studies using Review Manager 5.3 (Cochrane Collabora- other studies did not qualify for MA as their intervention, tion, Copenhagen). Intervention effects for individual assessment time points, and outcome measures were het- studies were summarized using standardized mean dif- erogeneous. (See Figure 2 for further information on the ferences (SMD) for continuous outcomes with two-sided study selection process.) 95% confidence intervals. An SMD value of 0.2 indicates a small effect, a value of 0.5 indicates moderate effect and Study characteristics 0.8 indicates a large effect.11 Data from studies that did A combined sample of 1,402 participants were included not have similar intervention types and timelines, or did not measure cognition within similar domains, could not in this review. Fifteen18–31,39 RCTs (68%), including two be appropriately combined through quantitative MA and © Canadian Physiotherapy Association, 2023

Akbari et al. Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors 15 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Figure 2 Preferred Reporting Items for Systematic Reviews (PRISMA) flow diagram of study selection. follow-up studies,23,26 and seven33–38 non-RCTs (31%) were Nineteen studies18–30,34–39 assessed social cognition (86%), included. See Table 1 for more details on each study three25,33,35 assessed executive function (14%), three24,25,32 included in this review. Populations across studies were assessed memory (14%), four24,25,30,32 assessed attention variable; the majority19,23–26,28–30,32,35,36,39 (59%) consisted of (18%), and one29 assessed psychomotor speed (5%). female participants with breast cancer (BC). Thirteen studies took place in an outpatient setting (59%), eight Risk of bias studies were conducted in an inpatient setting (36%), and Risk of bias was assessed using the RoB 2.0 tool, one was in a combination of both (5%). ROBINS-I, or NOS where appropriate (Figure 3). Overall The PA interventions across studies were variable. risk of bias was determined to be high in all studies but Nine studies18,22,24,31,34,37,38 (41%) delivered a combination one,37 which demonstrated moderate risk of bias. of resistance and aerobic exercises, four studies28,29,35,36 (18%) delivered a yoga-based intervention, and five stud- The GRADE quality of evidence was considered very ies,25,29,32,37,39 (23%) delivered either resistance or aerobic low for each outcome related to PA compared to no/usual exercises to the intervention group. Of the studies that care and low frequency PA compared to high frequency used comparison groups, most18,20–28,30–32,39 (77%) com- PA, primarily due to high risk of bias within each study. pared PA to usual care or no intervention. The durations See online Appendices 3, 4, and 5. of interventions ranged from 3 to 26 weeks. To evaluate cognition, 15 studies18–23,26–28,31,34,36–39 (68%) used self-re- Synthesis and analysis of results port measures only, two studies32,33 (9%) used only objec- tive outcome measures, and five studies24,25,29,30,35 (23%) Social cognition used both self-report and objective outcome measures. Nineteen studies used outcome measures assessing social cognition in survivors undergoing chemother- apy.18–30,34–39 Nine studies18–22,24,27,30,39 investigated the effects © Canadian Physiotherapy Association, 2023

16 Physiotherapy Canada, Volume 75, Number 1 Table 1 Summary of Included Studies Activity type: Intervention Activity type: https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Reference Study design Sample size Cancer type group Control group Outcome measure Adamsen37 Prospective study using a 115  Mixed AT and RT N/A EORTC-QLQ-C30  Adamsen22 one-group design   Backman39 RCT 269 Mixed Same as Adamsen, 2006.   UC EORTC-QLQ-C30  Baumann32  Randomized pilot study 77 EORTC-QLQ-C30  BC and colorectal AT (walking). Supervised UC Bland19 d2 test of attention cancer and home. Memo test Bolam23  Wilde Intelligence test Prospective non-RCT  17 BC RT Not described EORTC-QLQ-C30 Bryant20   Carayol24 2-arm RCT  31 BC AT (treadmill, ergometer, Same intervention PFS Fitzpatrick31  elliptical), RT and balance applied after EORTC-QLQ-C30 Fukushima34 Galantino35 (supervised and at home)  chemotherapy PROMIS Gokal25 2-y follow-up to an RCT  N: See Mijwel BC See Mijwel 2018  — Multidimensional fatigue 2018 inventory Henke18 Follow-up period: See EORTC QLQ-C30 Komatsu36 Test of Attentional Zhang31 Mijwel 2019  Performance Mijwel21  Montreal Cognitive Mijwel26 RCT 18 ALL AT (walking or bike) UC Assessment EORTC QLQ-C30 Oechsle38 AML and RT  Oechsle27  CogState: speed, 2-armed, RCT 143 BC AT (walking, jogging, UC accuracy, errors Perceived cognition cycling, swimming) and   Questionnaire Stroop RT forwards and backwards digit span in WAIS III  Longitudinal feasibility 15 BC and Tracked PA  Same as IG SART  study  44   WAIS block design  Longitudinal observational 4 Colorectal cancer  Low frequency CFQ study  AT and RT EORTC QLQ-C30/LC13 Case-series Mixed AT (Ergometer) and RT  N/A CFQ BC Yoga (supervised and at Revised-PFS home)   PFS RCT 50 BC AT (walking) UC EORTC-QLQ-C30    PFS EORTC-QLQ-C30 Prospective RCT 46 Lung Cancer AT (walking) and RT UC   Breathing: ACBT  EORTC QLQ-C13    BC Yoga (at home)  — EORTC-QLQ-C30 Ovarian cancer AT and RT UC Prospective feasibility study  21   BC RCT 72     BC 3-arm RCT 240 Mixed RT-HITT  UC Mixed AT-HITT(cycle ergometer,   elliptical, or treadmill)  — See Mijwel 2018  12 mo follow-up to an RCT N: see Mijwel Follow-up period: Health N/A 2018 counselling UC Tracked PA Cross-sectional 53 AT (bicycle ergometer) Prospective randomized 58 and RT pilot study  (Continued ) © Canadian Physiotherapy Association, 2023

Akbari et al. Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors 17 Table 1 (Continued) Activity type: Intervention Activity type: https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 Reference Study design Sample size Cancer type group Control group Outcome measure Rahmani28 Quasi-experimental design 24 BC Yoga and Breathing No intervention EORTC-QLQ-C30 with pre-test, post-test,   EORTC-QLQ-BR23 Schmidt30 control group (RCT) 81 BC AT: indoor bike  Schmidt 3-arm RCT 101 BC RT Not described EORTC-QLQ-C30  ME29   RT Muscle relaxation D2 test of attention Prospective RCT EORTC-QLQ-C30  trail-making test AT = aerobic training; RT = resistance training; N/A = not applicable; EORTC-QLQ-C30 = European Organization for Research and Treatment of Cancer Quality of Life Questionnaire-Core 30; RCT = randomized controlled trial; UC = usual care; BC = breast cancer; PFS = Piper Fatigue Scale; ALL = Acute Lymphocytic Leukemia; AML = Acute Myeloid Leukemia; PROMIS = Patient Reported Outcome Measurement Information System; PA = physical activity; IG = intervention group; SART = Sustained Attention to Response Task; WAIS = Wechsler Adult Intelligence Scale; CFQ = Cognitive Failures Questionnaire; ACBT = active cycle of breathing technique; EORTC QLQ-LC13 = European Organization for Research and Treatment of Cancer Quality of Life Questionnaire-Lung Cancer 13; HITT = high intensity interval training; EORTC-QLQ-C13 = European Organization for Research and Treatment of Cancer Quality of Life Questionnaire-Core13; EORTC-QLQ-BR23 = European Organization for Research and Treatment of Cancer Quality of Life Questionnaire-Breast Cancer 23. Figure 3 Risk of bias summary: Review authors’ judgments about each risk of bias item presented across a) 15 included randomized controlled trials using the Cochrane Risk of Bias 2.0 assessment tool, b) 3 included non-randomized controlled trials using the Cochrane Risk of Bias in Non-randomized Studies of Interventions assessment tool, and c) 4 included single-group cohort studies using the Newcastle-Ottawa Scale. © Canadian Physiotherapy Association, 2023

18 Physiotherapy Canada, Volume 75, Number 1 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 of a PA intervention on social cognition compared to usual case series and found that three out of four participants care. Five of those studies18–22 had similar intervention had improved CogState error scores. However, the effects parameters to combine in a MA. When combined, there of PA on cognition cannot be inferred as no statistical was a statistically significant small effect in social cognition analysis was performed. that favoured the PA group compared to usual care (SMD 0.23 (95% CI: 0.04, 0.42), p = 0.020, z = 2.34). Heterogeneity Memory between studies was low (2 = 1.91, p = 0.75, I2 = 0%). See Three studies24,25,32 assessed memory in participants Figure 4 for the forest plot. with cancer undergoing chemotherapy. Two studies25,32 Thirteen of the studies assessing social cognition were reported a statistically significant improvement in mem- RCTs; 11 used the European Organization for Research and ory following exercise. Using forwards digit span of the Treatment of Cancer Quality of Life Questionnaire-Core Wechsler Adult Intelligence Scale-III, one RCT25 of 50 par- 30 (EORTC QLQ-C30),18,21–24,26–30,39 one used the Patient ticipants reported statistically significant between-group Reported Outcome Measurement Information System (calculated mean change: 1.0, 95% CI: 0.4, 1.7) differ- (PROMIS),20 one used the Cognitive Failures Questionnaire ences that favoured exercise. Baumann and colleagues32 (CFQ),25 and one used the Revised Piper Fatigue Scale.31 Of assessed memory using the Wilde intelligence sub-test these studies, one had significant within-group findings.24 in 17 survivors and reported statistically significant with- Rahmani and colleagues24 reported a significant increase in-group (p = 0.049) and between-group (p = 0.048) differ- in social cognition in the IG after 8 weeks (calculated ences that favoured the PA group. mean difference: 12.5, 95% CI: 3.9, 21.1). Attention Two RCTs found significant between-group differences Four studies24,25,30,32 assessed attention in participants in social cognition favouring the IG post-intervention.21,24 Mijwel and colleagues reported a difference in cognition with cancer undergoing chemotherapy. Three studies24,30,32 favouring the RT-HIIT group compared to CG at 16 weeks reported a statistically significant improvement in atten- (calculated mean difference: 8.63, 95% CI: 1.11, 16.14).21 tion following PA. One RCT24 of 143 participants found a Carayol and colleagues assessed social cognition in 143 statistically significant between-group difference in atten- survivors and reported a mean difference of 8.48 (95% CI: tion using Test of Attentional Performance (mean differ- 3.13, 13.8).24 All other within- and between-group find- ence: −0.29, 95% CI: −0.48, −0.09) that favoured exercise at ings were statistically non-significant. 12 weeks, however, no significant differences were main- tained at the six month and one year follow-up.24 Two30,32 Three non-RCTs34,36,37 assessed social cognition, two34,37 studies reported significant within-group differences using the EORTC QLQ-C30, and one36 using the CFQ. Of using the D2 test of attention; one RCT30 with a sample size these, there were no significant within- or between-group of 81 participants in the resistance group (calculated mean findings post-intervention. difference: 16.3, 95% CI: 1.4, 31.3), and one non-RCT,32 with 17 survivors, in the IG only (p = 0.017). Baumann and Executive function colleagues32 also found significant between-group differ- Three studies25,33,35 assessed executive function in ences favouring the PA intervention group (p = 0.019). female participants with BC undergoing chemotherapy. Psychomotor speed One RCT with a sample size of 50 participants found no Only one RCT of 101 survivors assessed psychomo- statistically significant between- or within-group dif- ferences in Stroop Interference scores.25 Fitzpatrick and tor speed in RT compared to a muscle-relaxation pro- colleagues33 a one-group design study with 15 survivors, gramme using the trail-making-test.29 Schmidt and performed regression analysis to determine a positive colleagues9 found statistically significant improvements association between Montreal Cognitive Assessment and (mean change: −10.2, 95% CI: −16.3, −4.2) in psychomotor METs scores. Galantino and colleagues35 conducted a speed in the RT group. Between-group and within-group Figure 4 Forest plot displaying meta-analysis of the effect of exercise on social cognition in cancer survivors undergoing combined resistance and aerobic exercise interventions at 6 to 18 weeks. © Canadian Physiotherapy Association, 2023

Akbari et al. Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors 19 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 findings in the muscle relaxation group were not statisti- physiotherapists should continue to encourage and help cally significant. to facilitate exercise programming for individuals with cancer receiving chemotherapy. DISCUSSION This review aimed to explore the effectiveness of exer- This study has several limitations that should be kept in mind when interpreting the results. Firstly, this SR was cise during chemotherapy on cognitive function in can- restricted to English studies which may have excluded arti- cer survivors. Based on the MA, a combined resistance cles written in other languages that fit our inclusion cri- and aerobic exercise programme during chemotherapy teria. Furthermore, many included studies implemented treatment produced a small positive effect on social cog- co-interventions to the exercise intervention such as diet nition compared to controls at short-term follow-up. The education, medications, and additional interventions majority of articles included interventions of combined provided by other care providers. Future research should aerobic and resistance training, studied BC survivors, and compare the individual effects of various interventions in assessed cognition through a self-report outcome mea- order to determine the active ingredients of the successful sure. High heterogeneity was observed in cancer types, programmes. There is also a lack of consistency regarding outcome measures, and interventions used within the the definition of cognition used in the literature, which studies included in this SR. Overall high risk of bias across leads to challenges when comparing interventions and included studies resulted in very low certainty of the outcomes. We recommend that future researchers focus effect of PA compared to usual care in survivors undergo- on assessing cognition as a primary aim, using validated ing chemotherapy. (Figure 4) outcome measures. This review team chose to use the Cambridge Cognition definition4 for its comprehensive- The parameters of the exercise interventions used in the ness. Future researchers should consider choosing simi- included studies varied greatly. However, our MA focused lar definitions to ensure clarity, consistency, and ease of on interventions which combined resistance and aerobic interpretation. Another limitation is the high risk of bias of activity exclusively. In comparison, an SR by Mishra and all included studies. Larger and more rigorously designed colleagues40 did not find a significant effect of exercise, RCTs should be used to strengthen findings and reduce including yoga, cycling, aerobic, and/or strengthening the impact of bias on those results. programmes, on measures of cognitive function in cancer survivors post-cancer treatment. Contrastingly, our MA CONCLUSIONS found a positive effect on cognitive function suggesting The results from this SR and MA demonstrated that that the type of exercise intervention and timing of inter- vention may have an impact on cognitive outcomes. Other PA, specifically combined resistance and aerobic exer- research has found results corroborating our findings.41 A cise, may provide benefit to social cognitive function in previous MA by Fang and colleagues41 found a small to survivors receiving chemotherapy. However, due to the moderate effect on self-reported cognitive function after high risk of bias of included studies these findings should exercise in individuals receiving non-chemotherapy can- be interpreted with caution. More research is required cer treatments. While there is still a lack of information to further confirm and determine optimal exercise to give specific parameter recommendations for cancer parameters to limit treatment-related side effects in this survivors to improve cognitive function, our MA suggests population. that a combination of aerobic and resistance exercise can improve social cognition compared to usual care when KEY MESSAGES performed during chemotherapy. What is already known on this topic Overall, this review provides evidence of the positive Physical activity is beneficial for physical and mental effect of PA during chemotherapy on social cognition for individuals with cancer. Based on the findings of this health. Chemotherapy can lead to deterioration of cogni- MA, it is recommended that cancer survivors engage in tive functioning, commonly known as ‘chemo fog’. Physi- combined aerobic and resistance exercise while under- cal activity performed at various time points in the cancer going chemotherapy for protective effects on cognition. treatment trajectory can improve physical health and Data from the MA provides valuable insight to experts cognitive outcomes. of physical rehabilitation, such as physiotherapists, on delivering effective care based on the timing of the What this study adds intervention during chemotherapy treatment. While the Our study reveals a positive effect of a combined resis- type of interventions used within the included studies were heterogeneous, no adverse events were reported in tance and aerobic exercise intervention on social cogni- any of the included studies, supporting the safety of PA tion functioning in survivors undergoing chemotherapy. during chemotherapy for this population.6,7 Therefore, Further investigation is warranted to determine the effect of various types of physical activity on cognition in a larger population of survivors. © Canadian Physiotherapy Association, 2023

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Akbari et al. Effect of Physical Activity During Chemotherapy on Cognitive Function in Cancer Survivors 21 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 32. Baumann FT, Drosselmeyer N, Leskaroski A, et al. 12-week resistance 37. Adamsen L, Quist M, Midtgaard J, et al. The effect of a training with breast cancer patients during chemotherapy: effects multidimensional exercise intervention on physical capacity, on cognitive abilities. Breast Care. 2011;6(2):142–3. https://doi. well-being and quality of life in cancer patients undergoing org/10.1159/000327505. chemotherapy. Support Care Cancer. 2006;14(2):116–27. https:// doi.org/10.1007/s00520-005-0864-x. Medline:16096771 33. Fitzpatrick TR, Edgar L, Holcroft C. Assessing the relationship between physical fitness activities, cognitive health, and 38. Oechsle K, Jensen W, Schmidt T, et al. Physical activity, quality quality of life among older cancer survivors. J Psychosoc Oncol. of life, and the interest in physical exercise programs in patients 2012;30(5):556–72. https://doi.org/10.1080/07347332.2012.703768. undergoing palliative chemotherapy. Support Care Cancer. 2011; Medline:22963183 19(5):613–19. https://doi.org/10.1007/s00520-010-0862-5. Medline:20352266 34. Fukushima T, Nakano J, Ishii S, et al. Low-intensity exercise therapy with high frequency improves physical function and mental and 39. Backman M, Wengström Y, Johansson B, et al. A randomized physical symptoms in patients with haematological malignancies pilot study with daily walking during adjuvant chemotherapy undergoing chemotherapy. Eur J Cancer Care (Engl). 2018;27(6): for patients with breast and colorectal cancer. Acta Oncologica. e12922. https://doi.org/10.1111/ecc.12922. Medline:30311313 2014;53(4):510–20. https://doi.org/10.3109/0284186x.2013.873820. Medline:24460069 35. Galantino ML, Greene L, Daniels L, et al. Longitudinal impact of yoga on chemotherapy-related cognitive impairment and quality of life 40. Mishra SI, Scherer RW, Snyder C, et al. Exercise interventions on in women with early stage breast cancer: A case series. EXPLORE. health-related quality of life for people with cancer during active 2012;8(2):127–35. https://doi.org/10.1016/j.explore.2011.12.001. treatment. Cochrane Database Syst Rev. 2012 Aug. https://doi. Medline:22385567 org/10.1002/14651858.cd008465.pub2. Medline:22895974 36. Komatsu H, Yagasaki K, Yamauchi H, et al. A self-directed home yoga 41. Fang Y-Y, Lee Y-H, Chan J-C, et al. Effects of exercise interventions programme for women with breast cancer during chemotherapy: on social and cognitive functioning of men with prostate cancer: A feasibility study: yoga for patients undergoing chemotherapy. Int A meta-analysis. Support Care Cancer. 2020;28(5):2043–57. https:// J Nurs Pract. 2016;22(3):258–66. https://doi.org/10.1111/ijn.12419. doi.org/10.1007/s00520-019-05278-y. Medline:31907651 Medline:26643264 © Canadian Physiotherapy Association, 2023

ONLINE APPENDIX 1: SEARCH STRATEGY FOR MEDLINE OVID (EPUB AHEAD OF PRINT, IN-PROCESS & OTHER NON-INDEXED CITATIONS, DAILY AND MEDLINE; 1946 TO CURRENT) https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 1. cancer*.mp. or Thyroid Cancer, Papillary/ 34. Leisure Activities/ or leisure activit*.mp. 2. exp Neoplasms/ or exp Breast Neoplasms/ or 35. stretches.mp. 36. qi gong.mp. oncolog*.mp. 37. chi gung.mp. 3. exp Neoplasm Metastasis/ or neoplasm*.mp. 38. walking.mp. or exp Walking/ 4. exp Liver Neoplasms/ or exp Carcinoma, Squamous 39. walk.mp. 40. bicycling.mp. or exp Bicycling/ Cell/ or carcinom*.mp. or exp 41. exp Hydrotherapy/ or hydrotherap*.mp. Carcinoma, Non-Small-Cell Lung/ or exp Carcinoma, 42. aquatic exercis*.mp. Hepatocellular/ or exp Lung Neoplasms/ 43. kinesiotherapy.mp. 5. exp Carcinoid Tumor/ or tumor*.mp. or exp Mixed 44. therapeutic exercis*.mp. Tumor, Malignant/ 45. moving therap*.mp. 6. tumour*.mp. or exp Skin Neoplasms/ 46. flexibility train*.mp. 7. Malignant Carcinoid Syndrome/ or malignan*.mp. 47. OR/18–46 or Carcinoid Tumor/ 48. chemobrain.mp. 8. exp Multiple Myeloma/ or exp Hematologic 49. chemo-brain.mp. Neoplasms/ or hematooncological.mp. 50. chemofog.mp. 9. exp Leukemia/ or exp Hematologic Neoplasms/ or 51. chemo-fog.mp. exp Antineoplastic Agents/ or hematooncological.mp. 52. exp Cognition Disorders/ or exp Cognition/ or 10. hematologic neoplasm*.mp. 11. exp Chemotherapy, Adjuvant/ or exp Antineoplastic cognition*.mp. Combined Chemotherapy Protocols/ or 53. cognitive function*.mp. chemotherap*.mp. 54. exp Cognitive Dysfunction/ or cognitive.mp. 12. exp Adenocarcinoma/ or chemo*.mp. or exp 55. cognitive impairment.mp. Carcinoma, Squamous Cell/ 56. neurocognition.mp. 13. metastatic.mp. 57. problem solving.mp. or exp Problem Solving/ 14. metastas*.mp. 58. exp Memory, Short-Term/ or exp Memory/ or 15. exp Antineoplastic Agents/ or antineoplastic agent*. mp. exp Memory Disorders/ or exp Spatial 16. antineoplastic*.mp. Memory/or memory.mp. or exp Memory, 17. OR/1–16 Long-Term/ 18. exp Exercise/ or exp Exercise Therapy/ or exercis*.mp. 59. attention.mp. or exp Attention/ 19. physical activit*.mp. 60. CRCI.mp. 20. sport*.mp. or exp Sports/ 61. cancer related cognitive impairment*.mp. 21. aerobic*.mp. 62. learning.mp. or exp Learning/ or exp Learning 22. strength train*.mp. Disorders/ 23. stretching.mp. 63. cognitive dysfunction*.mp. 24. yoga.mp. or exp Yoga/ 64. executive function*.mp. 25. tai chi.mp. or exp Tai Ji/ 65. memory disorder*.mp. 26. tai ji.mp. 66. spatial learning.mp. or exp Spatial Learning/ 27. chi kung.mp. 67. cognition disorder*.mp. 28. qigong.mp. or exp Qigong/ 68. cognitive disorder*.mp. 29. exp Resistance Training/ or resistance train*.mp. 69. OR/18–46 30. exercise therap*.mp. 70. OR/47–67 31. mindfulness-based exercis*.mp. 71. 17 AND 68 AND 69 32. pilates.mp. 72. animals/ not humans/ 33. recreation.mp. or exp Recreation/ 73. 71 not 72 Physiotherapy Canada 2023; 75(1); 1; doi:10.3138/ptc-2021-0032 1



























26 Physiotherapy Canada, Volume 75, Number 1 Table 2 Unadjusted Univariate Analysis of Relationships Between Exercise and Outcomes of Spinal Surgery Participant group, no. (%)* p -value (comparison across https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 No Exercise; Infrequent Exercise; Regular Exercise; the 3 groups) Outcome n  = 995 n  = 245 n  = 963 Adverse events 64 (6.4) 17 (6.9) 49 (5.1) 0.345 Intraoperative adverse event 16 (1.6) 3 (1.4) 10 (1.0) 0.242 Surgical site infection or wound complication 67 (6.7) 25 (10.2) 41 (4.3)† < 0.001 Postoperative medical adverse event 28 (2.8) 6 (2.5) 18 (1.9) 0.388 Adverse event after discharge from hospital 205 (20.6) 49 (20.0) 141 (14.6)† 0.002 Any adverse event Hospital length of stay 2.6 (3.6) 2.7 (3.6) 2.2 (2.5)‡ < 0.001 Hospital LOS, d, mean (SD) 436 (43.8) 97 (39.6) 350 (36.3)† 0.008 Hospital prolonged LOS above median LOS Functional outcomes 3.7 (2.9) 3.7 (2.8) 4.1 (2.8) 0.145 Improvement in pain (NPRS scores) from baseline to 12 mo, mean (SD) 18.1 (25.2) 19.3 (24.0) 19.4 (23.9) 0.688 Improvement in health-related quality of life (EQ-5D scores) from baseline to 12 mo, mean (SD) 23.4 (20.7) 23.6 (19.0) 23.2 (17.4) 0.976 Improvement in low back–related disability (ODI scores) from baseline to 12 mo, mean (SD) * Unless otherwise indicated. † Represents statistically significant difference of the noted subgroup when compared to the other groups after Bonferroni adjustment (p < 0.01). ‡ Represents statistically significant difference of the noted subgroup when compared to the other groups after Tukey’s honestly significant difference test (p < 0.05). LOS = length of stay; NPRS = 11-point Numeric Pain Rating Scale; EQ-5D = Euroqol 5D questionnaire ODI = Oswestry Disability Index. in the Regular Exercise group compared with those in the savings when extrapolated to the thousands of patients other two groups. who undergo this surgery and whether there are specific subgroups who would more substantially benefit. The final multivariable general linear regression model to predict hospital length of stay included the follow­ Our findings are not surprising. Previous studies have ing covariates: gender, age, Charlson Comorbidity Index reported similar evidence for other surgical procedures, score, treatment with physiotherapy before surgery, including abdominal and cancer surgery.1,4,12–14 One post-secondary education, PHQ-9 score, and duration of notable difference is that for people undergoing spinal symptoms. This model demonstrated that the adjusted surgery, the primary condition of pain or motor deficits mean hospital length of stay was significantly lower for requiring surgery may be construed as a barrier to pre­ patients in the Regular Exercise group (mean 2.2 days) operative exercise. However, in our study patient sample, compared with patients in the other two groups combined there was no relationship between preoperative exercise (mean 2.5 days; p = 0.03). A similar multivariable logistic frequency and pain intensity (NPRS score) or presence of regression model demonstrated no difference between motor deficits. This finding suggests that spinal surgery participant groups related to prolonged hospital length of patients as a group are, on average, able to overcome pain stay (adjusted OR 0.84, 95% CI: 0.70, 1.01; p = 0.06). and motor deficits to engage in exercise. Further, a study of a spinal surgical prehabilitation programme found that DISCUSSION the intervention group showed no increase in pain scores Our results indicate that patients who reported exer­ or the need for analgesics.15 We did note that our regular exercise group had less preoperative low back–related cising twice or more per week before lumbar fusion spi­ disability (ODI scores), which may reflect the higher pre­ nal surgery had better immediate postoperative hospital operative function in activities of patients who exercised outcomes than those who exercised less. After adjusting regularly. for confounding factors, we determined that preoper­ ative exercise was associated with significantly lower The understanding that a link exists between preoper­ adverse event rates and shorter hospital length of stay, ative exercise and postoperative outcomes can lead to the although the length of stay was only reduced by 0.5 days. development of new approaches to improve the quality This study is the first to demonstrate these findings in a of perioperative surgical care. Assessment of physical fit­ multicentre analysis with prospectively collected data. ness prior to surgery may lead to better risk stratification Further research is required to determine whether this and assist in surgical and perioperative decision-making. shorter hospital length of stay results in meaningful cost However, no research efforts have determined the optimal © Canadian Physiotherapy Association, 2023

Lawrence et al. Beneficial Effects of Preoperative Exercise on the Outcomes of Lumbar Fusion Spinal Surgery 27 https://utpjournals.press${contentReq.requestUri} - Horizon College Physiotherapy <[email protected]> - Sunday, June 25, 2023 11:51:20 PM - IP Address:43.246.243.214 amount of preoperative physical fitness. Better prognosti­ the statistical differences we observed are partially due to cation of outcomes and risk of adverse events could lead the large sample size and may represent only modest clin­ to better-informed shared decision-making as to whether ical differences. Future research to specifically assess if to proceed with a surgical intervention, the anticipated certain baseline characteristics are associated with stron­ extent of the surgery, and the most appropriate postop­ ger effects of exercise on outcomes may help identify spe­ erative care pathway. Early decision-making is especially cific patient subgroups to target for prehabilitation. important for elective spinal surgery. CONCLUSION Many hospitals worldwide are incorporating prehabil­ This study is the first to evaluate the effect of preop­ itation programmes to optimize physical fitness prior to surgery.1,13 Most studies evaluating the impact of preha­ erative exercise using a nationwide spinal surgery reg­ bilitation on postoperative outcomes have not included istry. Although exercise is a first line of treatment for low spinal surgeries. However, a randomized clinical trial of 60 back pain, most of the lumbar spinal surgery patients in patients undergoing elective lumbar spinal surgery found our study self-reported being nearly or completely inac­ that a 6- to 8-week physiotherapist-supervised home exer­ tive. Inactivity was associated with poorer postoperative cise prehabilitation programme improved outcomes and surgical outcomes, including longer lengths of stay and shortened hospital stays with no increase in complica­ higher adverse event rates. Although we tried to adjust for tions.15 Another study of spinal surgery prehabilitation, confounding factors, future research is required to assess which involved a 197-patient randomized controlled trial, whether more accurate measures of preoperative fitness concluded that pre-surgery physiotherapy decreased pain (e.g., personal electronic fitness trackers) can better prog­ and risk avoidance behavior and improved psychological nosticate outcomes to allow for improved personalized well-being and quality of life, and that higher physical clinical decision-making and whether interventions such activity levels prior to surgery led to higher activity levels as prehabilitation can improve outcomes. In addition, at 1-year post-surgery.16 future studies should evaluate the potential cost savings associated with improved preoperative exercise prescrip­ At the time of this study, no multicentre studies on the tion to determine whether these interventions are cost-ef­ effect of preoperative exercise had been done. Even in fective. Nonetheless, given the general health benefits and the absence of formal prehabilitation programmes in the the potential for improved surgical outcomes, physio­ CSORN centres, we were able to demonstrate a strong therapists and other health care providers should counsel positive relationship between regular preoperative exer­ lumbar fusion spinal surgery patients on the importance cise and physiotherapy treatment during the 6 months prior of preoperative physical activity. to surgery and improved postoperative patient outcomes. Our findings suggest that incorporating preoperative phys­ KEY MESSAGES iotherapy can lead to better outcomes for patients. What is already known on this topic The results of our study should be interpreted with Lumbar fusion spinal surgeries are associated with caution. This ambispective study relied on self-reported assessments of exercise, which can be inaccurate. The high rates of adverse events. Identifying modifiable risk CSORN questionnaire items define exercise poorly, and factors that are associated with adverse events can pro­ patient responses may not accurately represent their level vide an opportunity for quality improvement. One poten­ of activity. There may be errors in patients’ self report of tially modifiable risk factor associated with poorer health exercise, and the questionnaire does not consider total outcomes is physical inactivity. physical activity (inclusive of activities such as house­ work or gardening). We were unable to determine a dose What this study adds response or minimum amount required with our crude This study is the first to evaluate the effect of preoper­ retrospective measure of physical activity. At the time of our analyses, our 1-year follow-up assessments were ative exercise using data in a nationwide spinal surgery limited (i.e., 1,563 of 2,203 were eligible for a 12-month registry. Less than 50% of elective lumbar fusion spinal follow-up assessment), which may have led to biased surgery patients self-reported engaging in regular preop­ results and insufficient power to determine significant erative exercise. We found that regular exercise (at least effects. The positive correlations we identified do not twice per week) prior to surgery was associated with sig­ imply causation. Although we adjusted for some con­ nificantly lower adverse event rates and shorter lengths founding factors, there may be other unmeasured fac­ of postoperative stays than infrequent or no exercise. tors potentially correlated with exercise in an individual patient that may be more important in determining their REFERENCES outcomes, which may affect the overall impact of exercise on any one particular outcome; thus, the benefit to clini­ 1. Myers JN, Fonda H. The impact of fitness on surgical outcomes: the cal decision-making of our results may be limited. Finally, case for prehabilitation. Curr Sports Med Rep. 2016;15(4):282–9. https://doi.org/10.1249/jsr.0000000000000274. Medline:27399826 © Canadian Physiotherapy Association, 2023

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