Application of estimand framework in ICH E9 (R1) to vaccine trials

References

• Baden, L. R., H. M. El Sahly, B. Essink, K. Kotloff, S. Frey, R. Novak, D. Diemert, S. A. Spector, N. Rouphael, C. B. Creech, et al. 2020. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. The New England Journal of Medicine. 384(5):403–416. doi:10.1056/NEJMoa2035389.
   PubMed Web of Science ®Google Scholar
• Bornkamp, B., K. Rufibach, J. Lin, Y. Liu, D. V. Mehrotra, S. Roychoudhury, H. Schmidli, Y. Shentu, and M. Wolbers. 2021. Principal stratum strategy: Potential role in drug development. Pharmaceutical Statistics 20 (4):737–751. doi:10.1002/pst.2104.
   PubMed Web of Science ®Google Scholar
• Broome, C. V. 1991. Vaccine efficacy determination. NIPH Annals 14 (2):219–221.
   PubMedGoogle Scholar
• Chan, I., W. Wang, and J. Heyse. 2018. Clinical trials: Vaccine development from: Encyclopedia of biopharmaceutical statistics CRC press. Accessed December 1, 2021. https://www.routledgehandbooks.com/doi/10.1201/9781351110273-130001226.
   Google Scholar
• Dunkle, L. M., R. Izikson, P. Patriarca, K. L. Goldenthal, D. Muse, J. Callahan, M. Cox, and P. S. C. 1. 2. Study Team. 2017. Efficacy of recombinant influenza vaccine in adults 50 years of age or older. The New England Journal of Medicine 376 (25):2427–2436. doi:10.1056/NEJMoa1608862.
   PubMed Web of Science ®Google Scholar
• Frangakis, C. E., and D. B. Rubin. 2002. Principal stratification in causal inference. Biometrics 58:21–29. doi:10.1111/j.0006-341x.2002.00021.x.
   PubMed Web of Science ®Google Scholar
• Gilbert, P. B., R. J. Bosch, and M. G. Hudgens. 2003. Sensitivity analysis for the assessment of causal vaccine effects on viral load in HIV vaccine trials. Biometrics 59 (3):531–541. doi:10.1111/1541-0420.00063.
   PubMed Web of Science ®Google Scholar
• Gilbert, P. B., B. E. Shepherd, and M. G. Hudgens. 2013. Sensitivity analysis of per-protocol time-to-event treatment efficacy in randomized clinical trials. Journal of the American Statistical Association 108 (503). doi: 10.1080/01621459.2013.786649.
   PubMed Web of Science ®Google Scholar
• Horne, A. D., P. A. Lachenbruch, and K. L. Goldenthal. 2000. Intent-to-treat analysis and preventive vaccine efficacy. Vaccine 19 (2–3):319–326. doi:10.1016/s0264-410x(00)00152-3.
   PubMed Web of Science ®Google Scholar
• Hudgens, M. G., P. B. Gilbert, and S. G. Self. 2004. Endpoints in vaccine trials. Statistical Methods in Medical Research 13 (2):89–114. doi:10.1191/0962280204sm356ra.
   PubMed Web of Science ®Google Scholar
• ICH (International Council for Harmonisation of Technical Requirements for Pharmaceuticals for Human Use). 2019. ICH E9 (R1) addendum on estimands and sensitivity analysis in clinical trials to the guideline on statistical principles for clinical trials. Accessed December 1, 2021. https://database.ich.org/sites/default/files/E9-R1_Step4_Guideline_2019_1203.pdf.
   Google Scholar
• Jin, M., and G. Liu. 2020. Estimand framework: Delineating what to be estimated with clinical questions of interest in clinical trials. Contemporary Clinical Trials 96:106093. doi:10.1016/j.cct.2020.106093.
   PubMed Web of Science ®Google Scholar
• Li, X., W. Wang, G. F. Liu, and I. Chan. 2011. Handling missing data in vaccine clinical trials for immunogenicity and safety evaluation. Journal of Biopharmaceutical Statistics 21 (2):294–310. doi:10.1080/10543406.2011.550111.
   PubMed Web of Science ®Google Scholar
• Lou, Y., M. P. Jones, and W. Sun. 2019. Assessing the ratio of means as a causal estimand in clinical endpoint bioequivalence studies in the presence of intercurrent events. Statistics in Medicine 38 (27):5214–5235. doi:10.1002/sim.8367.
   PubMed Web of Science ®Google Scholar
• Luna, J., M. Plata, M. Gonzalez, A. Correa, I. Maldonado, C. Nossa, D. Radley, S. Vuocolo, R. M. Haupt, and A. Saah. 2013. Long-term follow-up observation of the safety, immunogenicity, and effectiveness of Gardasil™ in adult women. Plos One 8 (12):e83431. doi:10.1371/journal.pone.0083431.
   PubMed Web of Science ®Google Scholar
• Mallinckrodt, C. H., J. Bell, G. Liu, B. Ratitch, M. O’kelly, I. Lipkovich, P. Singh, L. Xu, and G. Molenberghs. 2020. Aligning estimators with estimands in clinical trials: Putting the ICH E9(R1) guidelines into practice. Therapeutic Innovation & Regulatory Science 54 (2):353–364. doi:10.1007/s43441-019-00063-9.
   PubMed Web of Science ®Google Scholar
• Plotkin, S. A. 2010. Correlates of protection induced by vaccination. Clinical and Vaccine Immunology 17 (7):1055–1065. doi:10.1128/CVI.00131-10.
   PubMed Web of Science ®Google Scholar
• Polack, F. P., S. J. Thomas, N. Kitchin, J. Absalon, A. Gurtman, S. Lockhart, J. L. Perez, G. Marc, E. D. Moreira, C. Zerbini, et al. 2020. Safety and efficacy of the BNT162b2 mRNA Covid-19 Vaccine. The New England Journal of Medicine 383 (27):2603–2615. doi:10.1056/NEJMoa2034577.
   PubMed Web of Science ®Google Scholar
• Ratitch, B., J. Bell, C. Mallinckrodt, J. W. Bartlett, N. Goel, G. Molenberghs, M. O’kelly, P. Singh, and I. Lipkovich. 2020. Choosing estimands in clinical trials: Putting the ICH E9(R1) into practice. Therapeutic Innovation & Regulatory Science 54 (2):324–341. doi:10.1007/s43441-019-00061-x.
   PubMed Web of Science ®Google Scholar
• Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. The New England Journal of Medicine 361 (23):2209–2220. doi:10.1056/NEJMoa0908492.
   PubMed Web of Science ®Google Scholar
• Richardson, A., M. G. Hudgens, P. B. Gilbert, and J. P. Fine. 2014. Nonparametric bounds and sensitivity analysis of treatment effects. Statistical Science 29 (4):596–618. doi:10.1214/14-STS499.
   PubMed Web of Science ®Google Scholar
• Rufibach, K. 2019. Treatment effect quantification for time-to-event endpoints-Estimands, analysis strategies, and beyond. Pharmaceutical Statistics 18 (2):145–165. doi:10.1002/pst.1917.
   PubMed Web of Science ®Google Scholar
• Saah, A., O. Bautista, A. Luxembourg, and G. Perez. Intention-to-prevent analyses for estimating human papillomavirus vaccine efficacy in clinical studies. 2017. Contemporary Clinical Trials Communications 7:189–193. doi:10.1016/j.conctc.2017.07.010.
   PubMedGoogle Scholar
• Unkel, S., M. Amiri, N. Benda, J. Beyersmann, D. Knoerzer, K. Kupas, F. Langer, F. Leverkus, A. Loos, C. Ose, et al. 2019. On estimands and the analysis of adverse events in the presence of varying follow-up times within the benefit assessment of therapies. Pharmaceutical Statistics 18 (2):166–183. doi:10.1002/pst.1915.
   PubMed Web of Science ®Google Scholar
• Villar, L., G. H. Dayan, J. L. Arredondo-García, D. M. Rivera, R. Cunha, C. Deseda, H. Reynales, M. S. Costa, J. O. Morales-Ramírez, G. Carrasquilla, et al. 2015. Efficacy of a tetravalent dengue vaccine in children in Latin America. The New England Journal of Medicine 372 (2):113–123. doi:10.1056/NEJMoa1411037.
   PubMed Web of Science ®Google Scholar
• WHO (World Health Organization). 2006. Guidelines to assure the quality, safety and efficacy of recombinant HPV virus-like particle vaccines. Accessed December 1, 2021. http://screening.iarc.fr/doc/WHO_vaccine_guidelines_2006.pdf.
   Google Scholar
• Yang, F., J. Wittes, and B. Pitt. 2019. Beware of on-treatment safety analyses. Clinical Trials 16 (1):63–70. doi:10.1177/1740774518812774.
   PubMed Web of Science ®Google Scholar