European Heart Journal - Quality of Care and Clinical Outcomes (2023) 9, 1–7 REVIEW https://doi.org/10.1093/ehjqcco/qcac070 European Society of Cardiology quality indicators for the prevention and Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 management of cancer therapy-related cardiovascular toxicity in cancer treatment G.A. Lee 1,† , S. Aktaa 2,3,4 , E. Baker1 , C.P. Gale2,3,4 , Israa F Yaseen5,6 , G. Gulati 7,8 , R. Asteggiano 9,10 , S. Szmit 11,12 , A. Cohen-Solal 13,14 , A. Abdin15 , W. Jurczak16 , P. Garrido Lopez 17 , A.L. Sverdlov18 , C.G. Tocchetti19 , A. Barac 20 , I. Parrini21 , P. Zamorano22 , Z. Iakobishvili23,24 , R. Pudil25 , L. Badimon26 , A.M. Kirby27 , A.H. Blaes 28 , D. Farmakis 29 , G. Curigliano30,31 , R. Stephens32 , A.R. Lyon33 and T. Lopez-Fernandez34 1 Division of Applied Technology for Clinical Care, Florence Nightingale Faculty of Nursing, Midwifery & Palliative Care, King’s College London, James Clerk Maxwell Building, 57 Waterloo Road, London SE1 8WA, UK; 2 Leeds Institute of Cardiovascular and Metabolic Medicine, University of Leeds, Leeds, UK; 3 Leeds Institute for Data Analytics, University of Leeds, Leeds, UK; 4 Department of Cardiology, Leeds Teaching Hospitals NHS Trust, Leeds, UK; 5 Baghdad Heart Center, Baghdad Teaching Hospital, Medical City, Baghdad, Iraq; 6 Scientific Council of Cardiology, Iraqi Board for Medical Specializations, Baghdad, Iraq; 7 Institute of Clinical Medicine, University of Oslo, Oslo, Norway, Division of Research and Innovation, Akershus University Hospital, Lørenskog, Norway; 8 Department of Cardiology, Division of Medicine, Oslo University Hospital, Ullevål, Oslo, Norway; 9 School of Medicine, Insubria University, Varese, Italy; 10 LARC (Laboratorio Analisi e Ricerca Clinica), C.so Venezia 10, Turin, Italy; 11 Department of Pulmonary Circulation, Thromboembolic Diseases and Cardiology, Centre of Postgraduate Medical Education, Otwock, Poland; 12 Institute of Hematology and Transfusion Medicine, Warsaw, Poland; 13 Research Medical Unit INSERM U-942, University of Paris, Paris, France; 14 Cardiology Department, Hôpitaux de Paris, Hôpital Lariboisière 2 Rue Ambroise Paré, Paris, France; 15 Department of Internal Medicine III, Cardiology, Angiology, Intensive Care Medicine, Saarland University Medical Center, Homburg, Germany; 16 MSC National Research Institute of Oncology, Garnarska 11, 31-115 Krakow, Poland; 17 Jefe Servicio Oncología Médica, Hospital Universitario Ramón y Cajal, Madrid, Spain; 18 Newcastle Centre of Excellence in Cardio-Oncology, Calvary Mater Newcastle, Hunter Medical Research Institute, John Hunter Hospital, University of Newcastle, NSW, Australia; 19 Cardio-Oncology Unit, Department of Translational Medical Sciences (DISMET), Center for Basic and Clinical Immunology Research (CISI), Interdepartmental Center for Clinical and Translational Research (CIRCET), Interdepartmental Hypertension Research Center (CIRIAPA), Federico II University, Naples, Italy; 20 Cardio-oncology Program, MedStar Heart and Vascular Institute, Washington DC, USA; 21 Department of Cardiology, Mauriziano Hospital, Turin, Italy; 22 University Hospital Ramon y Cajal, Madrid, Spain; 23 Department of Community Cardiology, Clalit Health Services, Tel Aviv Jaffa, Israel; 24 Faculty of Health Sciences, Ben Gurion University of the Negev, Beersheba, Israel; 25 University Hospital Hradec Králové, Sokolská 5005, Hradec Králové, Czech Republic; 26 IIBSant Pau, Hospital de la Santa Creu i Sant Pau, CiberCV, Barcelona, Spain; 27 Royal Marsden NHS Trust & Institute of Cancer Research, London, UK; 28 Division of Hematology/Oncology/Transplantation, University of Minnesota, Minneapolis, MN, USA; 29 University of Cyprus Medical School, Nicosia, Cyprus; 30 Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy; 31 IRCCS, European Institute of Oncology, Milan, Italy; 32 Patient Advocate, London, UK; 33 National Heart and Lung Institute, Imperial College London, and Cardio-Oncology Service, Royal Brompton Hospital, London, UK; and 34 Cardiology department, La Paz University Hospital, IdiPAZ Research Institute, Madrid, Spain Received 12 October 2022; accepted 21 October 2022; online publish-ahead-of-print 31 October 2022 Aims To develop quality indicators (QIs) for the evaluation of the prevention and management of cancer therapy-related cardiovascular toxicity. ............................................................................................................................................................................................ Methods and We followed the European Society of Cardiology (ESC) methodology for QI development which comprises (i) identifying results the key domains of care for the prevention and management of cancer therapy-related cardiovascular toxicity in patients on cancer treatment, (ii) performing a systematic review of the literature to develop candidate QIs, and (iii) selecting of the final set of QIs using a modified Delphi process. Work was undertaken in parallel with the writing of the 2022 ESC Guidelines on Cardio-Oncology and in collaboration with the European Haematology Association, the European Society for Therapeutic Radiology and Oncology and the International Cardio-Oncology Society. In total, 5 main and 9 secondary QIs were selected across five domains of care: (i) Structural framework, (ii) Baseline cardiovascular risk assessment, † Corresponding author. Tel: +44207 8483201, Email: Gerry.lee@kcl.ac.uk ‡ Developed in collaboration with the Heart Failure Association of the European Society of Cardiology. © The Author(s) 2022. Published by Oxford University Press on behalf of the European Society of Cardiology. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com 2 G. Lee et al. (iii) Cancer therapy related cardiovascular toxicity, (iv) Predictors of outcomes, and (v) Monitoring of cardiovascular complications during cancer therapy. ............................................................................................................................................................................................ Conclusion We present the ESC Cardio-Oncology QIs with their development process and provide an overview of the scientific rationale for their selection. These indicators are aimed at quantifying and improving the adherence to guideline- recommended clinical practice and improving patient outcomes. Quality indicators r Cardio-oncology r r r ............................................................................................................................................................................................ Keywords Assessment Treatment Cancer therapy-related cardiovascular toxicity r Outcomes Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 Introduction the developed indicators. The target population was defined as patients with an established cardiovascular disease prior to commencing cancer Cardio-oncology has emerged in recent years as a distinct entity that treatment and those who were at high risk of cardiovascular complications requires specialist expertise different from that provided by cardiology during or after receiving cancer treatment. and/or oncology services. The complexity of the acute cardiovascular For each domain, the measurement period was specified to clarify the presentations from cytotoxic, targeted and immunotherapies neces- timepoint at which each QI is measured. These timepoints extended from sitates co-operation between various specialists to ensure holistic the period before starting cancer treatment (for the assessment of the delivery of care that aims to identify and mitigate the risks of cardio- cardiovascular toxicity risks) to the long-term follow up after the comple- vascular complications during and after cancer therapy.1–3 The greater tion of cancer therapy (for the identification of potential cardiovascular numbers of cancers that are treated with cardiotoxic therapies, along- consequences of cancer treatment). side the better screening for cancer therapy-related cardiovascular Further specifications were provided for individual QIs including a toxicity (CTR-CVT), create a need to develop tools to measure the numerator, which is the criteria by which the QI is accomplished and a de- quality of cardio-oncology care and capture outcomes. nominator, which is the eligibility criteria for the QIs. Given that structural The European Society of Cardiology (ESC) strives to develop QIs are binary measurements of the availability of certain services, only suites of quality indicators (QIs) for its Clinical Practice Guidelines numerators are defined for the structural QIs. Both main and secondary to facilitate the implementation of these evidenced-based guidelines QIs were developed based on the voting scores on the validity and the and enable the quantification of the quality-of-care delivery.4 Thus, feasibility of the candidate QIs. in parallel with the writing of the 2022 ESC Guidelines on cardio- oncology developed in collaboration with the European Hematology Association (EHA), the European Society for Therapeutic Radiol- Systematic review methods ogy and Oncology (ESTRO) and the International Cardio-Oncology Search strategy Society (IC-OS): Developed by the task force on cardio-oncology We conducted a systematic review of published literature using the Pre- of the European Society of Cardiology (ESC),5 and in collaboration ferred Reporting for Systematic Review and Meta-Analyses (PRISMA) with the European Haematology Association (EHA), the European statement.6 A search strategy was developed using keywords and medical Society for Therapeutic Radiology and Oncology (ESTRO) and the subject headings that included Cardio-toxicity, Cardio-oncology, Oncol- International Cardio-Oncology Society (IC-OS), a group of domain ogy, Haemato-oncology, Quality indicators and Outcome measures and experts in cardio-oncology was formed to construct QIs that span medical subject headings such as ‘Cancer’, ‘oncological treatment’, ‘risk the breadth of cardio-oncology care and capture the key aspects of factor’ and ‘quality indicator’ (Supplementary material online, Table S1). its care delivery and outcomes that are relevant to patients. We developed separate search strategies for MEDLINE and Embase via OVID® using an iterative process incorporating result of hand searching Methods from reference lists and grey literature. We used the ESC methodology for the development of QIs which com- prises the following steps: (i) identifying key domains of care for the prevention and management of CTR-CVT in patients on cancer treat- Eligibility criteria ment, (ii) undertaking a systematic literature review to develop candidate Studies included were those that evaluated the cardiovascular conse- QIs, and (iii) selecting of the final set of QIs using a modified Delphi quences of cancer therapy in adult patients (>18 years old) who have process.4 Structural QIs are the measures that evaluate care quality at been treated with at least one cardiotoxic treatment at any point in- institutional level, while process QIs are the measures that evaluate care cluding chemotherapy, radiotherapy and immunotherapy. We included quality at the patient level. Furthermore, QIs allow the capture of relevant randomised controlled trials and observational studies as well as consensus outcomes that have an association with the quality-of-care delivery. documents that are published in English between 01 January 2015 and 10 September 2021. We excluded systematic reviews, meta-analysis, confer- Members of the development group ence abstracts and case reports. Studies with no defined intervention or The development group comprised Task Force members of the 2022 outcome measures were also excluded. Guidelines on Cardio-Oncology, members of the ESC QI Committee, nominees from the Council of Cardio-Oncology (CO-Council) and the ESC Patient Forum, as well as international experts in Cardio-oncology Study selection field including representatives from IC-OS, EHA, and ESTRO. Endnote X9 (Clarivate Analytics, London, UK) was used to manage refer- ences and remove duplicates. Two authors (EB and GL) independently Target population and domains of care examined the abstracts of the retrieved studies which were assessed The group initially defined the target population for whom the QIs will against the eligibility criteria. Disagreements were resolved through a third apply and the key domains of cardio-oncology care which encompass reviewer (SA) and full text article review. Prevention and management of cancer therapy-related cardiovascular toxicity in cancer treatment. 3 Identification Records removed before Records identified from: screening: Medline (n=1494) Embase (n=1208) Duplicate records removed Other sources (n=6) (n=1081) Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 Records excluded: Relevance (n = 1017) Records screened Conference abstract (n=1627) (n=82) Methodology (n=148) Screening Reports excluded: No CV or clinical outcomes (n Reports assessed for eligibility = 171) (n=380) Children (n = 16) Single arm/no comparison (n=49) Methodology (n=79) Not Cancer (n=1) Included Studies included in review (n=64) Figure 1 Preferred Reporting for Systematic Review and Meta-Analyses Flow Chart for selection of included studies. PRISMA, Preferred Reporting for Systematic Review and Meta-Analyses. Data extraction of 4–6 meant that the QI is of an uncertain validity/feasible; and ratings of For each included study, the systematic review team extracted the 7–9 meant that the QI is valid/feasible. For each candidate QI, the median definitions of the target population, intervention(s), comparison(s) and and the mean deviation from the median were calculated to evaluate the outcome measure(s). Data were collated using an Excel spreadsheet. central tendency and the dispersion of the votes. Indicators, with median scores ≥7 for validity, ≥4 for feasibility, and with minimal dispersion, were included in the final set of QIs. The development group was asked to Data synthesis modify the phrasing of the candidate QIs to reach consensus on the Modified Delphi process The modified Delphi approach was used inclusion of the indicator in the final set. to evaluate the candidate QIs derived from the literature review.4 The members of the group were made aware of the ESC criteria for QI development to standardize the voting process, and each candidate QI Results was ranked by each panellist on a 9-point ordinal scale for both validity Systematic review results and feasibility using an online questionnaire (See supplement for criteria The domains of care identified were: (i) Structural framework, table). Two rounds of voting were conducted using the Delphi process (ii) Baseline cardiovascular risk assessment, (iii) CTR-CVT, (iv) Predic- with a series of virtual meetings between April 2021 until July 2022 to tors of outcomes and (v) Monitoring of cardiovascular complications discuss the voting results and address concerns and queries. during cancer therapy. The literature search retrieved 1081 articles, of which 64 met the inclusion criteria (see Figure 1). These studies were Analysis of voting results The 9-point ordinal scale used for voting used to extract 33 candidate QIs which were included in the first implied that ratings of 1–3 meant that the QI is not valid/feasible; ratings voting round. In total 5 (15%) of the candidate QIs were included as 4 G. Lee et al. Table 1: ESC Cardio-oncology quality indicators for the management of patients with cancer or cancer survivors ............................................................................................................................................................................................................ DOMAIN 1: Structural framework Main 1: Healthcare centres providing cancer treatment with available resources for patient education including dedicated health care professionals to optimise patient ability to manage self-care during and after treatment. Numerator: centres providing cancer treatment with available resources for patient education including dedicated health care professionals to optimise patient ability to manage self-care during and after treatment. Secondary 1: Healthcare centres providing cancer treatment with an available MDT for cardio-oncology. MDT should comprise as a minimum an oncologist**, a cardiologist and a specialist nurse* . Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 Numerator: centres providing cancer treatment with an available MDT for cardio-oncology. DOMAIN 2: Baseline cardiovascular risk assessment Main 2.1: Proportion of patients considered for cancer treatment$ who are evaluated for prior history/clinical evidence of cardiovascular condition (including heart failure, coronary artery disease, arrhythmias, history of pulmonary embolism or deep vein thrombosis) prior to treatment Numerator: patients considered for cancer treatment who are evaluated for a prior history of cardiovascular condition (including heart failure, coronary artery disease, arrhythmias, pulmonary embolism, or deep vein thrombosis) prior to treatment Denominator: patients considered for cancer treatment Measurement period: prior to treatment Main 2.2: Proportion of patients considered for cancer treatment who have their modifiable cardiovascular risk factors (Diabetes Mellitus, Hypertension etc) identified prior to treatment Numerator: patients considered for cancer treatment who have their modifiable cardiovascular risk factors (Diabetes Mellitus, Hypertension, etc) identified Denominator: patients considered for cancer treatment Measurement period: prior to treatment Main 2.3: Proportion of patients considered for cancer treatment who have been engaged in shared decision-making when deciding treatment strategy Numerator: patients considered for cancer treatment who have been engaged in shared decision-making when deciding treatment strategy Denominator: patients considered for cancer treatment Measurement period: prior to treatment Secondary 2.1: Proportion of patients considered for cardiotoxic cancer treatment# who have an assessment of their cardiovascular risk using diagnostic tools Numerator: patients considered for cardiotoxic cancer treatment who have an assessment of their cardiovascular risk assessment using diagnostic tools Denominator: patients considered for cancer treatment Measurement period: prior to treatment DOMAIN 3: Cancer Therapy Related Cardiovascular Toxicity Main 3: Annual rate of hospitalisation due to cancer therapy related cardiovascular toxicity Numerator: patients on or have recently been on cancer treatment who are hospitalised due to cancer therapy related cardiovascular toxicity Denominator: patients on or have recently been on cancer treatment Measurement period: during or after treatment Secondary 3.1: Proportion of patients with symptoms and/or signs of cancer therapy related cardiovascular toxicity during/after cardiotoxic cancer treatment who have a cardiovascular assessment Numerator: patients with symptoms and/or signs of cancer therapy related cardiovascular toxicity during/after cardiotoxic cancer treatment who have a cardiovascular assessment Denominator: patients with symptoms of cancer treatment-related toxicity during/after cardiotoxic cancer treatment Measurement period: during and after treatment Secondary 3.2: Proportion of patients at high risk& for cancer therapy related cardiovascular toxicity who are followed up after the completion of cardiotoxic cancer treatment to evaluate for adverse cardiac events Numerator: patients at high risk& for cancer therapy related cardiovascular toxicity who are followed up after the completion of cardiotoxic cancer treatment to evaluate for adverse cardiac events Denominator: patients after the completion of cardiotoxic cancer treatment Measurement period: 1 and 5 years after treatment Secondary 3.3: Proportion of patients who have a cardiovascular risk assessment 1 year after the completion of cardiotoxic cancer treatment# Numerator: patients who have a cardiovascular risk assessment 1 year after the completion of cardiotoxic cancer treatmentˆ Denominator: patients within 1 year of the completion of cardiotoxic cancer treatment Measurement period: 1 year after treatment DOMAIN 4: Predictors of outcomes Secondary 4.1: Proportion of patients who develop symptomatic HFrEF during cancer treatment and are prescribed medications such as beta blockers, ACEI/ARB/ARNI, MRA and SGLT2 inhibitors Numerator: patients who develop HF during cancer treatment and are prescribed beta blockers, ACEI/ARB/ARNI, MRA and SGLT2 inhibitors Prevention and management of cancer therapy-related cardiovascular toxicity in cancer treatment. 5 Table 1 Continued. ............................................................................................................................................................................................................ DOMAIN 4: Predictors of outcomes Denominator: patients who develop HF during cancer treatment Measurement period: during and after treatment Secondary 4.2: Proportion of patients treated with anthracyclines or HER2 targeted therapies and develop asymptomatic moderate or severe CTRCD during cancer treatment who are prescribed beta blockers and/or ACEI/ARB Numerator: patients treated with anthracyclines or HER2 targeted therapies and develop asymptomatic moderate or severe CTRCD during cancer treatment who are prescribed beta blockers and/or ACEI/ARB Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 Denominator: patients treated with anthracyclines or HER2 targeted therapies and develop asymptomatic moderate or severe CTRCD during cancer treatment Measurement period: during treatment DOMAIN 5: Monitoring of cardiovascular complications during cancer therapy Secondary 5.1: Proportion of patients on HER2-targeted therapies who have their cardiovascular assessment every 3 months during the first year of treatment Numerator: patients on HER2-targeted therapies who have their cardiovascular assessment every 3 months during the first year of treatment Denominator: patients on HER2-targeted therapies Measurement period: during & after treatment Secondary 5.2: Proportion of patients on TKI, including BTKi, who have their blood pressure assessed at every clinical visit. Numerator: Proportion of patients on TKI (including BTKi) who have their blood pressure assessed at every clinical visit. Denominator: patients on TKI (including BTKi) Measurement period: during and after treatment * Ideally MDT should also involve a radiologist, surgeon, palliative care expert, physiotherapist, pharmacist, psychologist, general practitioner, and dietitian. & High-risk patients are those with >10% risk of future cardiovascular toxicity according to HFA-ICOS risk assessment (Lyon AR et al. 2020). # Cardiotoxic cancer treatment is defined as any cancer treatment with potential cardiovascular side effects. ˆ Assessment includes an echocardiography (at baseline and within 12 months after completing treatment and include a documentation of LVEF and GLS assessment), cardiac troponins and NPs in high and very high-risk patients (at baseline, before every anthracycline cycle and 3 and 12 months after therapy completion). **Oncologist includes three specialists: medical oncologist, haematologist and radiation oncologist. $ Cancer treatment includes chemotherapy, targeted agents, hormone therapies, immune therapies, and radiation therapy. main QIs. Of the remaining indicators, 19 (58%) were excluded and comprehensive clinical assessment may identify patients at higher risk 9 (27%) were considered in a second Delphi round and included as and highlight strategies to mitigate this risk (Secondary 2.1). secondary QIs (see Table 1). Domain 3: Cancer therapy related cardiovascular toxicity Quality indicators (CTR-CVT) Given CTR-CVT is associated with cardiovascular mortality during Domain 1: Structural framework and after cancer treatment,7,8 capturing the annual rate of hospital- Two QIs have been selected in this domain. The first is a main QIs isation due to CTR-CVT has been selected as a main QIs (Main 3). that captures the need for dedicated healthcare professionals for After starting cancer treatment, it is important to perform a compre- cardio-oncology patients (Main 1). The second defines the appropri- hensive cardiovascular assessment for patients developing signs and/or ate composition of a multidisciplinary team in this setting (Secondary symptoms of CTR-CVT (Secondary 3.2). However, CTR-CVT can 1), which should consist of at least an oncologist, cardiologist and a sometimes be asymptomatic and at various time points. As such, two specialist nurse. The team should ideally have access to other services QIs have been selected to ensure appropriate follow up for high-risk such as a radiologist, surgeon, haematologist, palliative care expert, individuals (Secondary 3.3) and within 3 months from the completion physiotherapist, pharmacist, psychologist, general practitioner, and of cancer treatment (Secondary 3.3).5,9 dietitian. Given the implementation of this QI may be challenging in some healthcare centres, it was included as a secondary one. Domain 4: Predictors of outcomes Heart failure and in particular heart failure with reduced Ejection Frac- Domain 2: Baseline cardiovascular risk assessment tion (HFrEF) is a well-documented complication of cancer treatment The QIs under this domain relate to the importance of a com- and patients should be closely monitored in the first year following prehensive cardiovascular assessment prior to commencing cancer completion of treatment.7,10 Early diagnosis is an important measure treatment. That is, the documentation of previous cardiovascular along with appropriate management with guideline-directed med- history (for instance, history or clinical evidence of venous thrombo- ical therapy including beta-blockers, renin-angiotensin-aldosterone embolism) (Main 2.1), as well as the identification of modifiable risk inhibitors, and sodium glucose co-transporter2 inhibitors (Secondary factors associated with cardiovascular complications such as diabetes 4.1).11 This QI has been aligned with the ESC guidelines for HF and and hypertension (Main 2.2). The other QI in this domain relates to the respective QI for HFrEF.12,13 The second QI in this domain is a the need to ensure that shared decision-making is discussed with more specific indicator that pertains to reducing the risk of anthra- the patient when determining the treatment strategy (Main 2.3). cycline and HER2 therapies by commencing prognostic treatment for In addition, the assessment of cardiovascular risk by performing a moderate or severe asymptomatic CTRCD (Secondary 4.2). 6 G. Lee et al. Domain 5: Monitoring of cardiovascular complications effects of cancer regimens and their effect on the cardiovascular during cancer therapy system. Whilst different types of cancer treatment may have an impact on the cardiovascular system, certain treatments are known to be more Supplementary material toxic than others.14 As such, close monitoring for patients on HER2 Supplementary material is available at European Heart Journal— therapies with a structured assessment to their side-effect profile Quality of Care and Clinical Outcomes online. may help identify and address these adverse events early (Secondary 5.1). For those on tyrosine kinase inhibitors, the assessment of blood Conflict of interest: G.L.: Grants: Horizon 2020. pressure at every visit (Secondary 5.2) may have a role in recognising S.A.- Educational events (Wondr medical), European Society of Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 the potential implications of this therapy.15 Cardiology. E.B.- Health Education England Post Doctoral Research Fellowship C.G.: BHF, NIHR, Horizon 2020, Daichii Sankyo NHS Joint Working Discussion Party, Abbott Diabetes, BMS/Pfizer. Honoraria: Astra Zeneca, Boston Scientific, Menarini, Raisio Group, Wondr Medical, Zydus. Boards: This document presents the ESC QIs for cardio-oncology and high- Amgen, Bayer, BMS, Boehringer Ingelheim, Chiesi Ltd, Daichii Sankyo, lights the breadth of this field which span across various clinical Menarini Diagnostics UK, iRhythm. Leadership: NICE indicator ad- settings. These indicators have been developed in parallel with the visory committee, Deputy Editor: EHJ Quality of Care and Clinical writing of the 2022 ESC guidelines on cardio-oncology and using Outcomes, Oxford University Press, Chair ESC Quality Indicator the ESC methodology.4,5 We have identified 5 domains of care for Committee. cardio-oncology and selected 5 main and 9 secondary QIs across G.G.: Honoraria: AstraZeneca, BMS, Roche, Orion Pharma, No- these domains. They include structural indicators of care quality such vartis. Leadership: Board member Norwegian Cardiology Society as the availability of a multi-disciplinary team, the benefits of which R.A.- Royalties from Springer. have been previously highlighted,16 as well as process and outcome S.S.: Amgen, Angelini, Astra Zeneca, BMS, Bayer, Gilead, Pfizer QIs, with particular focus on shared decision-making as a key factor A.C. Solal: Vifor, Novartis, MSD, Bayer, Sanofi, Boehringer Ingel- for successful treatment.17 heim, Amgen, Servier Cardio-oncology is expanding with increasing patient population P.G.: Honoraria: Advisory Role: Abbvie, Amgen, Astra Zeneca, and complexity, creating a need to standardize the methods by which Bayer, BMS, Daichi, GSK, Janssen, Lilly, MSD, Novartis, Pfizer, Roche, care delivery is measured and outcomes captured given the existing Takeda, Sanofi. Speaker: Janssen, MSD, Novartis, Medscape, Takeda, variation and the room for improvement.18 Calls have been made TouchTime. Support attending meetings: Astra Zeneca, BMS. Leader- to establish designated cardio-oncology centres across Europe in line ship: ESMO Council member with the growing number of patients in need for specialists’ input and A S.: Future Leader Fellowships (Awards IDs 101 918 & 106 025). multidisciplinary management plans.19 Patients on cancer treatment Medical Research Future Fund (Australia). NSW Department of are at a higher risk for developing cardiovascular complications, and Health, RACE Oncology. Honoraroa: Celgene Pty Ltd, BMS, Novar- a number of strategies may help mitigate these risks. As such, we its, BMS, AstraZeneca, Boehringer Ingelheim. Leadership: ESC, Joint combined existing evidence with expert consensus to develop a suite Cardiac Society of Australia and New Zealand and Clinical Oncol- of QIs for patients considered for or receiving cancer treatment. ogy Society of Australia Cardio-Oncology Working Group, Global We are not aware of any previous initiative that aimed to develop Cardio-Oncology Registry. internationally endorsed set of QIs for cardio-oncology patients. The C.G.T.: Italian Ministero della Salute RF 2016, VivaLyfe, Univers widespread implementation of these indicators enables the conduc- Formazione, Menarini, Amgen. Patients: P75NTR. tion of meaningful comparative analyses across different centres and P.Z.: Honoraria: Novo Nordisk, Novaris, Philips, Bayer, Medtronic, regions to highlight disparities and standardise patient care. Besides, Amgen. the integration of these QIs into a system of data collection may Z.L.: Grants: Novo-Nordisk. Consulting fees: Bayer, Pfizer, facilitate the establishment of a unified registry for cardio-oncology Boehringer Ingelheim. Honoraria: Pfizer, AstraZeneca. that may help generate evidence and monitor patterns of care delivery R.P.: Grants: COOPERATIO, AZV NV19-02-00297. Honoraria: over time. Novartis, Boehringer Ingelheim. Although there are obvious strengths to the study, there are some L.B.: Grants: AstraZeneca, EU H2020, EU IMI, EU Sudoe. Hono- limitations that need to be acknowledged. The final QIs were de- raria: Amarin, Novartis, Pfizer. Patients: gly-APOJ, IVSTATINa, DJ1F. termined by expert opinion via the Delphi process and therefore Data Safety Monitoring: Novartis, Novo Nordisk, Pfizer, Sanofi, Inter- reflects the views of the Working Group members. However, this was national Aspirin Foundation, FICYE. Leadership: ESC. preceded by a systematic literature review and the Delphi method A.K.: President of European Society of Radiation Therapy and used to independently record experts’ votes to select the QIs and Oncology also we applied the ESC criteria to standardise the voting process. D.F.: Consulting fees: Abbott, Bayer, Boehringer-Ingelheim, Leo The feasibility of the QIs is an issue and relates to organisational G.C.- Grants: Merck, AstraZeneca. Consulting fees: Roche, BMS, barriers and limited resources in clincial practice across Europe. We Novartis, Lily, Pfizer, Seagen, Ellipsis, Gilead, Merck, Celcuity, Daichii acknowledge that there is a variance of resources and the QIs may not Sankyo. Leadership: ESMO Council be feasible currently but can be used to standardise care and improve R.S. Honoraria: for being a cancer patient advocate working as a patient services in the future. volunteer in cancer research A.R.L.: ARL is supported by the Fondation Leducq Network of Excellence in Cardio-Oncology. Speaker, advisory board or con- Conclusions sultancy fees and/or research grants from Pfizer, Novartis, Servier, We present the ESC Cardio-Oncology QIs along with the devel- AstraZeneca, Bristol Myers Squibb, GSK, Amgen, Takeda, Roche, opment process and provide an overview of the scientific rationale Janssens-Cilag Ltd, Clinigen Group, Eli Lily, Eisai Ltd, Ferring Phar- for their selection. These indicators are aimed at quantifying and maceuticals, Boehringer Ingelheim, Akcea Therapeutics, Myocardial improving adherence to guideline-recommended clinical practice and Solutions, iOWNA Health and Heartfelt Technologies Ltd improving patient outcomes with particular focus on the cardio-toxic T.L-F: Philips, Janssem, Incyte Prevention and management of cancer therapy-related cardiovascular toxicity in cancer treatment. 7 Data availability 9. Lyon AR., Dent S, Stanway S, Earl H, Brezden-Masley H, Cohen-Solal A et al. Baseline cardiovascular risk assessment in cancer patients scheduled to receive cardiotoxic The data underlying this article are available and in the online supple- cancer therapies: a position statement and new risk assessment tools from the mentary material. Cardio-Oncology Study Group of the Heart Failure Association of the European So- ciety of Cardiology in collaboration with the International Cardio-Oncology Society. References Eur J Heart Fail 2020;22:1945–1960. 10. Vo JB, Ramin C, Barac A, Berrington de Gonzalez A, Veiga L. Trends in heart disease 1. Gevaert SA, Halvorsen S, Sinnaeve PR, Sambola A, Gulati G, Lancellotti P et al. mortality among breast cancer survivors in the US, 1975-2017. Breast Cancer Res Evaluation and management of cancer patients presenting with acute cardiovascular Treat. 2022;192:611–622. doi: 10.1007/s10549-022-06515-5. disease: a consensus document of the Acute CardioVascular Care (ACVC) association 11. Lewinter C, Nielsen TH, Edfors LR, Linde C, Bland JM, LeWinter M et al. A systematic and the ESC council of Cardio-Oncology—Part 1: acute coronary syndromes and review and meta-analysis of beta-blockers and renin—angiotensin system inhibitors Downloaded from https://academic.oup.com/ehjqcco/article/9/1/1/6783158 by Fundacio Biblioteca Josep Laporte user on 06 October 2023 acute pericardial diseases. EHJ Acute CV Care 2021;10:947–959. for preventing left ventricular dysfunction due to anthracyclines or trastuzumab in 2. Gevaert SA, Halvorsen S, Sinnaeve PR, Sambola A, Gulati G, Lancellotti P et al. Evalua- patients with breast cancer. Eur Heart J 2022; 43:2562–2569. https://doi.org/10.1093/ tion and management of cancer patients presenting with acute cardiovascular disease: eurheartj/ehab843 a Consensus Document of the Acute CardioVascular Care (ACVC) association and 12. McDonagh TA, Metra M, Adamo M, Gardner RS, Baumbach A, Böhm M et al. ESC the ESC council of Cardio-Oncology - Part 2: Acute Heart Failure, Acute myocardial Scientific Document Group. 2021 ESC Guidelines for the diagnosis and treatment of diseases, Acute Venous Thromboembolic Diseases and Acute Arrhythmias. EHJ Acute acute and chronic heart failure: Developed by the Task Force for the diagnosis and CV Care 2022. In press. treatment of acute and chronic heart failure of the European Society of Cardiology 3. Zamorano JL, Lancellotti P, Rodriguez Muñoz D, Galderisi M, Habib G, Lenihan DJ (ESC) With the special contribution of the Heart Failure Association (HFA) of the et al., Authors/Task Force Members; ESC Committee for Practice Guidelines (CPG). ESC. Eur Heart J 2021; ehab368. ESC Position Paper on cancer treatments and cardiovascular toxicity developed under 13. Aktaa S, Polovina M, Rosano G, Abdin A, Anguita M, Lainscak M et al. European the auspices of the ESC Committee for Practice Guidelines: The Task Force for cancer Society of Cardiology quality indicators for the care and outcomes of adults with treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). heart failure. Developed by the Working Group for Heart Failure Quality Indicators Eur Heart J 2016 37:2768–2801. in collaboration with the Heart Failure Association of the European Society of 4. Aktaa S, Batra G, Wallentin L, Erlinge D, James S, Ludman P et al. European Society Cardiology. Eur J Heart Fail 2022;24:132–142. of Cardiology methodology for the development of quality indicators for the quan- 14. Morelli MB, Bongiovanni C, Da Pra S, Miano C, Sacchi F, Lauriola M et al. tification of cardiovascular care and outcomes. Eur Heart J Qual Care Clin Outcomes. Cardiotoxicity of Anticancer Drugs: Molecular Mechanisms and Strategies for Car- 2022; 8:4–13. dioprotection. FRONT CARDIOVASC MED 2022:9:847012. doi: 10.3389/fcvm.2022. 5. Lyon AR, López-Fernández T, Couch LS, Asteggiano R, Aznar MC, Bergler-Klein J 847012 et al., ESC Scientific Document Group, 2022 ESC Guidelines on cardio-oncology 15. Roa-Chamorro R, Jaén-Águila F, Puerta-Puerta J.M, Torres-Quintero L, González- developed in collaboration with the European Hematology Association (EHA), the Bustos P, Mediavilla-García JD et al. Arterial hypertension assessment in a population European Society for Therapeutic Radiology and Oncology (ESTRO) and the In- with chronic myeloid leukemia. Sci Rep 11:14637 (2021). https://doi.org/10.1038/ ternational Cardio-Oncology Society (IC-OS): Developed by the task force on s41598-021-94127-2 cardio-oncology of the European Society of Cardiology (ESC), EHJ, 2022; ehac244, 16. Boriani G, Lee G, Parrini I, Lopez-Fernandez T, Lyon AR, Suter T et al. Anticoagulation https://doi.org/10.1093/eurheartj/ehac244 in patients with atrial fibrillation and active cancer: an international survey on patient 6. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic management. Eur J Prev Cardiol 2021;28:611–621. reviews and meta-analyses: the PRISMA statement. BMJ 2009;339:b2535. 17. Hendriks J, Lee G. Shared decision making—The patient on the forefront of care 7. López-Sendón J, Álvarez-Ortega C, Auñon PZ, Soto AB, Lyon AR, Farmakis D et al., coordination. Eur Heart J Qual Care Clin Outcomes 2020:6:231–233. https://doi.org/ on behalf of the CARDIOTOX Registry Investigators, Classification, prevalence, and 10.1093/ehjqcco/qcaa039 outcomes of anticancer therapy-induced cardiotoxicity: the CARDIOTOX registry, 18. Asteggiano R, Aboyans V, Lee GA, Salinger S, Richter D. Cardiology care delivered Eur Heart J 2020; 41:1720–1729. https://doi.org/10.1093/eurheartj/ehaa006 to cancer patients: The results of a questionnaire survey by the Council for Cardio 8. Henson KE, McGale P, Darby SC, Parkin M, Wang Y, Taylor CW et al. Cardiac Oncology and Council for Cardiology Practice of the European Society of Cardiology. mortality after radiotherapy, chemotherapy and endocrine therapy for breast cancer: Eur Heart J 2020;41:205–206. Cohort study of 2 million women from 57 cancer registries in 22 countries. Int J 19. Lancellotti P, Suter TM, Galderisi M, Lyon AR, Van der Meer P et al. Cardio-Oncology Cancer. 2020;147:1437–1449. doi: 10.1002/ijc.32908. Epub 2020 Mar 4. Erratum in: Services: rationale, organization, and implementation: A report from the ESC Cardio- Int J Cancer. 2021 Feb 1;148(3):E1. Oncology council. Eur Heart J 2019; 40:1756–1763.