How to make cardiology clinical trials more inclusive.


Journal

Nature medicine
ISSN: 1546-170X
Titre abrégé: Nat Med
Pays: United States
ID NLM: 9502015

Informations de publication

Date de publication:
14 Oct 2024
Historique:
received: 10 04 2024
accepted: 28 08 2024
medline: 15 10 2024
pubmed: 15 10 2024
entrez: 14 10 2024
Statut: aheadofprint

Résumé

Cardiovascular clinical trials continue to under-represent children, older adults, females and people from ethnic minority groups relative to population disease distribution. Here we describe strategies to foster trial representativeness, with proposed actions at the levels of trial funding, design, conduct and dissemination. In particular, trial representativeness may be increased through broad recruitment strategies and site selection criteria that reflect the diversity of patients in the catchment area, as well as limiting unjustified exclusion criteria and using pragmatic designs that minimize research burden on patients (including embedded and decentralized trials). Trial communications ought to be culturally appropriate; engaging diverse people with lived experience in the co-design of some trial elements may foster this. The demographics of trialists themselves are associated with participant demographics; therefore, trial leadership must be actively diversified. Funding bodies and journals increasingly require the reporting of sociodemographic characteristics of trial participants, and regulatory bodies now provide guidance on increasing trial diversity; these steps may increase the momentum towards change. Although this Perspective focuses on the cardiovascular trial context, many of these strategies could be applied to other fields.

Identifiants

pubmed: 39402268
doi: 10.1038/s41591-024-03273-3
pii: 10.1038/s41591-024-03273-3
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. Springer Nature America, Inc.

Références

Vilcant, V., Ceron, C., Verma, G., Zeltser, R. & Makaryus, A. N. Inclusion of under-represented racial and ethnic groups in cardiovascular clinical trials. Heart Lung Circ. 31, 1263–1268 (2022).
doi: 10.1016/j.hlc.2022.06.668 pubmed: 35850910
Filbey, L. et al. Improving representativeness in trials: a call to action from the Global Cardiovascular Clinical Trialists Forum. Eur. Heart J. 44, 921–930 (2023).
doi: 10.1093/eurheartj/ehac810 pubmed: 36702610 pmcid: 10226751
Jin, X. et al. Women’s participation in cardiovascular clinical trials from 2010 to 2017. Circulation 141, 540–548 (2020).
doi: 10.1161/CIRCULATIONAHA.119.043594 pubmed: 32065763
Cholesterol Treatment Trialists’ Collaboration Efficacy and safety of statin therapy in older people: a meta-analysis of individual participant data from 28 randomised controlled trials. Lancet 393, 407–415 (2019).
Au, M. et al. A systematic review of sex-specific reporting in heart failure clinical trials: trial flow and results. J. Am. Coll. Cardiol. Adv. 1, 100079 (2022).
Wei, S. et al. Factors associated with racial and ethnic diversity among heart failure trial participants: a systematic bibliometric review. Circ. Heart Fail. 15, e008685 (2022).
doi: 10.1161/CIRCHEARTFAILURE.121.008685 pubmed: 34911363
Tahhan, A. S. et al. Enrollment of older patients, women, and racial/ethnic minority groups in contemporary acute coronary syndrome clinical trials: a systematic review. JAMA Cardiol. 5, 714–722 (2020).
doi: 10.1001/jamacardio.2020.0359 pubmed: 32211813
Cherubini, A. et al. The persistent exclusion of older patients from ongoing clinical trials regarding heart failure. Arch. Intern. Med. 171, 550–556 (2011).
doi: 10.1001/archinternmed.2011.31 pubmed: 21444844
Michos, E. D. & Van Spall, H. G. C. Increasing representation and diversity in cardiovascular clinical trial populations. Nat. Rev. Cardiol. 18, 537–538 (2021).
doi: 10.1038/s41569-021-00583-8 pubmed: 34108677
National Academies of Sciences, Engineering, and Medicine. Improving Representation in Clinical Trials and Research: Building Research Equity for Women and Underrepresented Groups (eds Bibbins-Domingo, K. & Helman, A.) (National Academies Press, 2022).
Packer, M. et al. Cardiovascular and renal outcomes with empagliflozin in heart failure. N. Engl. J. Med. 383, 1413–1424 (2020).
doi: 10.1056/NEJMoa2022190 pubmed: 32865377
Zannad, F. et al. SGLT2 inhibitors in patients with heart failure with reduced ejection fraction: a meta-analysis of the EMPEROR-Reduced and DAPA-HF trials. Lancet 396, 819–829 (2020).
doi: 10.1016/S0140-6736(20)31824-9 pubmed: 32877652
Lam, C. S. P. et al. Regional and ethnic influences on the response to empagliflozin in patients with heart failure and a reduced ejection fraction: the EMPEROR-Reduced trial. Eur. Heart J. 42, 4442–4451 (2021).
doi: 10.1093/eurheartj/ehab360 pubmed: 34184057 pmcid: 8599078
Rathore, S. S., Wang, Y. & Krumholz, H. M. Sex-based differences in the effect of digoxin for the treatment of heart failure. N. Engl. J. Med. 347, 1403–1411 (2002).
doi: 10.1056/NEJMoa021266 pubmed: 12409542
Mihan, A., Pandey, A. & Van Spall, H. G. C. Mitigating the risk of artificial intelligence bias in cardiovascular care. Lancet Digit. Health https://doi.org/10.1016/S2589-7500(24)00155-9 (2024).
Bodicoat, D. H. et al. Promoting inclusion in clinical trials—a rapid review of the literature and recommendations for action. Trials 22, 880 (2021).
doi: 10.1186/s13063-021-05849-7 pubmed: 34863265 pmcid: 8643184
Goldberg, E. M. et al. Using social media for clinical research: recommendations and examples from the Brown-Lifespan Center for Digital Health. J. Med. Internet Res. 24, e35804 (2022).
doi: 10.2196/35804 pubmed: 35700012 pmcid: 9237766
Mihan, A. & Van Spall, H. G. C. Interventions to enhance digital health equity in cardiovascular care. Nat. Med. 30, 628–630 (2024).
doi: 10.1038/s41591-024-02815-z pubmed: 38355972
Fultinavičiūtė, U. AI benefits in patient identification and clinical trial recruitment has challenges in sight. Clinical Trials Arena https://www.clinicaltrialsarena.com/features/ai-clinical-trial-recruitment/ (2022).
Grover, N. & Coulter, M. Insight: big pharma bets on AI to speed up clinical trials. Reuters https://www.reuters.com/technology/big-pharma-bets-ai-speed-up-clinical-trials-2023-09-22/ (2023).
Kretschmer, M., Kretschmer, T., Peukert, A. & Peukert, C. The risks of risk-based AI regulation: taking liability seriously. SSRN https://doi.org/10.2139/ssrn.4622405 (2023).
Strumberger, S. EU AI Act: the latest updates on the world’s first comprehensive AI regulation laws. Thomson Reuters https://legalsolutions.thomsonreuters.co.uk/blog/2023/12/12/ai-act-the-worlds-first-comprehensive-laws-to-regulate-ai/#:~:text=In%20April%202021%2C%20the%20European,mean%20more%20or%20less%20regulation (2024).
Ali, M. R., Lawson, C. A., Wood, A. M. & Khunti, K. Addressing ethnic and global health inequalities in the era of artificial intelligence healthcare models: a call for responsible implementation. J. R. Soc. Med. 116, 260–262 (2023).
doi: 10.1177/01410768231187734 pubmed: 37467785 pmcid: 10469966
Green, B. L., Murphy, A. & Robinson, E. Accelerating health disparities research with artificial intelligence. Front. Digit. Health 6, 1330160 (2024).
doi: 10.3389/fdgth.2024.1330160 pubmed: 38322109 pmcid: 10844447
Gilstrap, L. G. et al. Epidemiology of cardiac amyloidosis-associated heart failure hospitalizations among fee-for-service Medicare beneficiaries in the United States. Circ. Heart Fail. 12, e005407 (2019).
doi: 10.1161/CIRCHEARTFAILURE.118.005407 pubmed: 31170802 pmcid: 6557425
Van Spall, H. G. C. et al. Knowledge to action: rationale and design of the Patient-Centered Care Transitions in Heart Failure (PACT-HF) stepped wedge cluster randomized trial. Am. Heart J. 199, 75–82 (2018).
doi: 10.1016/j.ahj.2017.12.013 pubmed: 29754670
Van Spall, H. G. C. et al. Effect of patient-centered transitional care services on clinical outcomes in patients hospitalized for heart failure: the PACT-HF randomized clinical trial. J. Am. Med. Assoc. 321, 753–761 (2019).
doi: 10.1001/jama.2019.0710
Zhu, J. W. et al. Incorporating cultural competence and cultural humility in cardiovascular clinical trials to increase diversity among participants. J. Am. Coll. Cardiol. 80, 89–92 (2022).
doi: 10.1016/j.jacc.2022.05.001 pubmed: 35772919
Van Spall, H. G., Toren, A., Kiss, A. & Fowler, R. A. Eligibility criteria of randomized controlled trials published in high-impact general medical journals: a systematic sampling review. J. Am. Med. Assoc. 297, 1233–1240 (2007).
doi: 10.1001/jama.297.11.1233
Van Spall, H. G. C. et al. A guide to implementation science for phase 3 clinical trialists: designing trials for evidence uptake. J. Am. Coll. Cardiol. (in the press).
Clinical and Translational Science Awards Consortium Community Engagement Key Function Committee Task Force on the Principles of Community Engagement. Principles of Community Engagement 2nd edn, Report No. NIH 11-7782 (US Department of Health and Human Services, 2011).
TRUST Consortium. Global code of conduct for research in resource-poor settings. European Research Council https://ec.europa.eu/info/funding-tenders/opportunities/docs/2021-2027/horizon/guidance/global-code-of-conduct-for-research-in-resource-poor-settings_he_en.pdf (2020).
DeFilippis, E. M. et al. Improving enrollment of underrepresented racial and ethnic populations in heart failure trials: a call to action from the Heart Failure Collaboratory. JAMA Cardiol. 7, 540–548 (2022).
doi: 10.1001/jamacardio.2022.0161 pubmed: 35319725 pmcid: 9098689
Taylor, C. J. et al. Research priorities in advanced heart failure: James Lind alliance priority setting partnership. Open Heart 7, e001258 (2020).
doi: 10.1136/openhrt-2020-001258 pubmed: 32606070 pmcid: 7328807
Van Spall, H. G. C. Exclusion of pregnant and lactating women from COVID-19 vaccine trials: a missed opportunity. Eur. Heart J. 42, 2724–2726 (2021).
doi: 10.1093/eurheartj/ehab103 pubmed: 33686419
Assadpour, E. & Van Spall, H. G. C. Pregnant and lactating women should be included in clinical trials for cardiovascular disease. Nat. Med. 29, 1897–1899 (2023).
doi: 10.1038/s41591-023-02416-2 pubmed: 37365348
Filbey, L., Khan, M. & Van Spall, H. G. Protection by inclusion: increasing enrollment of women in cardiovascular trials. Am. Heart J. Cardiol. Res. Pr. 13, 100091 (2022).
Zannad, F. et al. Patient partnership in cardiovascular clinical trials. Eur. Heart J. 43, 1432–1437 (2022).
doi: 10.1093/eurheartj/ehab835 pubmed: 34897413
Centre for Ethnic Health Research. Increasing diversity in research. Centre for Ethnic Health Research https://ethnichealthresearch.org.uk/increasing-diversity-in-research/ (2023).
Spertus, J. A. et al. The SGLT2 inhibitor canagliflozin in heart failure: the CHIEF-HF remote, patient-centered randomized trial. Nat. Med. 28, 809–813 (2022).
doi: 10.1038/s41591-022-01703-8 pubmed: 35228753 pmcid: 9018422
Usman, M. S. et al. The need for increased pragmatism in cardiovascular clinical trials. Nat. Rev. Cardiol. 19, 737–750 (2022).
doi: 10.1038/s41569-022-00705-w pubmed: 35581337 pmcid: 9112643
Gross, A. M. et al. Selumetinib in children with inoperable plexiform neurofibromas. N. Engl. J. Med. 382, 1430–1442 (2020).
doi: 10.1056/NEJMoa1912735 pubmed: 32187457 pmcid: 7305659
Newton, W. External control arms: when can historical data substitute for placebos? Clinical Trials Arena https://www.clinicaltrialsarena.com/features/external-control-arms/?cf-view&cf-closed (2022).
Thorlund, K., Dron, L., Park, J. J. H. & Mills, E. J. Synthetic and external controls in clinical trials—a primer for researchers. Clin. Epidemiol. 12, 457–467 (2020).
doi: 10.2147/CLEP.S242097 pubmed: 32440224 pmcid: 7218288
Khan, M. S. et al. Leveraging electronic health records to streamline the conduct of cardiovascular clinical trials. Eur. Heart J. 44, 1890–1909 (2023).
doi: 10.1093/eurheartj/ehad171 pubmed: 37098746
Erlinge, D. et al. Bivalirudin versus heparin in non-ST and ST-segment elevation myocardial infarction—a registry-based randomized clinical trial in the SWEDEHEART registry (the VALIDATE-SWEDEHEART trial). Am. Heart J. 175, 36–46 (2016).
doi: 10.1016/j.ahj.2016.02.007 pubmed: 27179722
Erlinge, D. et al. Bivalirudin versus heparin monotherapy in myocardial infarction. N. Engl. J. Med. 377, 1132–1142 (2017).
doi: 10.1056/NEJMoa1706443 pubmed: 28844201
Mohammad, M. A. et al. Development and validation of an artificial neural network algorithm to predict mortality and admission to hospital for heart failure after myocardial infarction: a nationwide population-based study. Lancet Digit. Health 4, e37–e45 (2022).
doi: 10.1016/S2589-7500(21)00228-4 pubmed: 34952674
Wester, A. et al. Bivalirudin versus heparin monotherapy in elderly patients with myocardial infarction: a prespecified subgroup analysis of the VALIDATE-SWEDEHEART trial. Circ. Cardiovasc. Inter. 13, e008671 (2020).
doi: 10.1161/CIRCINTERVENTIONS.119.008671
Venetsanos, D. et al. Sex-related response to bivalirudin and unfractionated heparin in patients with acute myocardial infarction undergoing percutaneous coronary intervention: a subgroup analysis of the VALIDATE-SWEDEHEART trial. Eur. Heart J. Acute Cardiovasc. Care 8, 502–509 (2019).
doi: 10.1177/2048872618803760 pubmed: 30351167
Berwanger, O. & Machline-Carrion, M. J. Digital health-enabled clinical trials in stroke: ready for prime time? Stroke 53, 2967–2975 (2022).
doi: 10.1161/STROKEAHA.122.037378 pubmed: 35770670
Jones, W. S. et al. Comparative effectiveness of aspirin dosing in cardiovascular disease. N. Engl. J. Med. 384, 1981–1990 (2021).
doi: 10.1056/NEJMoa2102137 pubmed: 33999548 pmcid: 9908069
Mackenzie, I. S. et al. Cardiovascular outcomes in adults with hypertension with evening versus morning dosing of usual antihypertensives in the UK (TIME study): a prospective, randomised, open-label, blinded-endpoint clinical trial. Lancet 400, 1417–1425 (2022).
doi: 10.1016/S0140-6736(22)01786-X pubmed: 36240838 pmcid: 9631239
Food and Drug Administration, Center for Drug Evaluation and Research & Center for Biologics Evaluation and Research. Adaptive Designs for Clinical Trials of Drugs and Biologics: Guidance for Industry (FDA, 2019).
Bouzalmate-Hajjaj, A., Massó Guijarro, P., Khan, K. S., Bueno-Cavanillas, A. & Cano-Ibáñez, N. Benefits of participation in clinical trials: an umbrella review. Int. J. Environ. Res. Public Health 19, 15368 (2022).
doi: 10.3390/ijerph192215368 pubmed: 36430100 pmcid: 9691211
Nunes, J. C., Rice, E. N., Stafford, R. S., Lewis, E. F. & Wang, P. J. Underrepresentation of ethnic and racial minorities in atrial fibrillation clinical trials. Circ. Arrhythm. Electrophysiol. 14, e010452 (2021).
doi: 10.1161/CIRCEP.121.010452 pubmed: 34789014
Martin, G., Mathur, R. & Naqvi, H. How can we make better use of ethnicity data to improve healthcare services? Br. Med. J. 380, 744 (2023).
doi: 10.1136/bmj.p744
Canadian Institutes of Health Research. Indigenous health research. CIHR https://cihr-irsc.gc.ca/e/52489.html (2023).
Clinical Trials Ontario. Streamlined ethics review. CTO https://ctontario.ca/programs/streamlined-research-ethics/ (2024).
Food and Drug Administration. Diversity Plans to Improve Enrollment of Participants from Underrepresented Racial and Ethnic Populations in Clinical Trials: Guidance for Industry—Draft. (FDA, 2022).
European Parliament & Council of the European Union. Regulation (EU) No 536/2014 of the European Parliament and of the Council of 16 April 2014 on Clinical Trials on Medicinal Products for Human Use, and Repealing Directive 2001/20/EC (Text with EEA relevance). Document no. 32014R0536 (European Union, 2014).
Sharma, G. et al. 10 recommendations to enhance recruitment, retention, and career advancement of women cardiologists. J. Am. Coll. Cardiol. 74, 1839–1842 (2019).
doi: 10.1016/j.jacc.2019.08.016 pubmed: 31582144
Whitelaw, S. et al. Trial characteristics associated with under-enrolment of females in randomized controlled trials of heart failure with reduced ejection fraction: a systematic review. Eur. J. Heart Fail. 23, 15–24 (2021).
doi: 10.1002/ejhf.2034 pubmed: 33118664
Denby, K. J. et al. Representation of women in cardiovascular clinical trial leadership. JAMA Intern. Med. 180, 1382–1383 (2020).
doi: 10.1001/jamainternmed.2020.2485 pubmed: 32865557 pmcid: 7489421
Eliya, Y. et al. Temporal trends and clinical trial characteristics associated with the inclusion of women in heart failure trial steering committees: a systematic review. Circ. Heart Fail. 14, e008064 (2021).
doi: 10.1161/CIRCHEARTFAILURE.120.008064 pubmed: 34281362
Van Spall, H. G. C. et al. Ending gender inequality in cardiovascular clinical trial leadership: JACC review topic of the week. J. Am. Coll. Cardiol. 77, 2960–2972 (2021).
doi: 10.1016/j.jacc.2021.04.038 pubmed: 34112322
Zhu, J. W. et al. Global representation of heart failure clinical trial leaders, collaborators, and enrolled participants: a bibliometric review 2000–20. Eur. Heart J. Qual. Care Clin. Outcomes 8, 659–669 (2022).
doi: 10.1093/ehjqcco/qcab058 pubmed: 34427651
Rubin, E. Striving for diversity in research studies. N. Engl. J. Med. 385, 1429–1430 (2021).
doi: 10.1056/NEJMe2114651 pubmed: 34516052
Borrelli, N. et al. Women leaders in cardiology. Contemporary profile of the WHO European region. Eur. Heart J. Open 1, oeab008 (2021).
doi: 10.1093/ehjopen/oeab008 pubmed: 35919091 pmcid: 9242062
Burgess, S. et al. Women in medicine: addressing the gender gap in interventional cardiology. J. Am. Coll. Cardiol. 72, 2663–2667 (2018).
doi: 10.1016/j.jacc.2018.08.2198 pubmed: 30466523
Capranzano, P. et al. Motivations for and barriers to choosing an interventional cardiology career path: results from the EAPCI Women Committee worldwide survey. EuroIntervention 12, 53–59 (2016).
doi: 10.4244/EIJY15M07_03 pubmed: 26151955
European Society of Cardiology. ESC gender policy. ESC https://www.escardio.org/static-file/Escardio/About%20the%20ESC/Documents/European%20Society%20of%20Cardiology%20Gender%20Policy.pdf (2022).
Ballarini, N. M. et al. Optimizing subgroup selection in two-stage adaptive enrichment and umbrella designs. Stat. Med. 40, 2939–2956 (2021).
doi: 10.1002/sim.8949 pubmed: 33783020 pmcid: 8251960

Auteurs

Faiez Zannad (F)

Université de Lorraine, Inserm Clinical Investigation Center at Institut Lorrain du Coeur et des Vaisseaux, Nancy, France. f.zannad@chru-nancy.fr.
University Hospital of Nancy, Nancy, France. f.zannad@chru-nancy.fr.

Otavio Berwanger (O)

George Institute for Global Health UK, London, UK.
Imperial College London, London, UK.

Stefano Corda (S)

Bayer Consumer Care, Basel, Switzerland.

Martin R Cowie (MR)

Division of Cardiovascular Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

Habib Gamra (H)

Cardiology A Department, Fattouma Bourguiba University Hospital, University of Monastir, Monastir, Tunisia.

C Michael Gibson (CM)

Baim Institute for Clinical Research, Harvard Medical School, Boston, MA, USA.

Alexandra Goncalves (A)

Bristol Myers Squibb, Cambridge, MA, USA.
University of Porto Medical School, Porto, Portugal.

Thomas Hucko (T)

Global Development, Amgen, Thousand Oaks, CA, USA.

Kamlesh Khunti (K)

Leicester Diabetes Centre, University of Leicester, Leicester, UK.

Maciej Kostrubiec (M)

Bristol Heart Institute, University Hospitals Bristol and Weston NHS Foundation Trust, Bristol, UK.
Department of Internal Medicine and Cardiology, The Medical University of Warsaw, Warsaw, Poland.

Bettina Johanna Kraus (BJ)

Medical Affairs, Boehringer Ingelheim International, Ingelheim, Germany.
Department of Internal Medicine I, University Hospital Würzburg, Würzburg, Germany.

Cecilia Linde (C)

Division of Cardiology, Department of Medicine, Karolinska Institutet and Karolinska Universitetssjukhuset, Stockholm, Sweden.

Thomas F Lüscher (TF)

Royal Brompton and Harefield Hospitals, Imperial College London and King's College London, London, UK.
Center for Molecular Cardiology, University of Zurich, Zurich, Switzerland.

Marion Mafham (M)

Clinical Trial Service Unit and Epidemiological Studies Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.

Richard Mindham (R)

European Society of Cardiology Patient Forum, London, UK.

Rebecca F Ortega (RF)

Women as One, Severna Park, MD, USA.

Eva Prescott (E)

Bispebjerg and Frederiksberg University Hospital, Copenhagen, Denmark.

Lehana Thabane (L)

Research Institute of St. Joseph's, St. Joseph's Healthcare, Hamilton, Ontario, Canada.
Department of Health Research Methods, Evidence, and Impact, McMaster University, Hamilton, Ontario, Canada.

Clyde Yancy (C)

Department of Internal Medicine, Division of Cardiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA.

André Ziegler (A)

Cardiovascular Diseases, Roche Diagnostics, Rotkreuz, Switzerland.

Harriette G C Van Spall (HGC)

Baim Institute for Clinical Research, Harvard Medical School, Boston, MA, USA.
Research Institute of St. Joseph's, St. Joseph's Healthcare, Hamilton, Ontario, Canada.
Department of Health Research Methods, Evidence, and Impact, McMaster University, Hamilton, Ontario, Canada.
Department of Medicine, Faculty of Health Sciences, McMaster University, Hamilton, Ontario, Canada.
Population Health Research Institute, Hamilton, Ontario, Canada.

Classifications MeSH