Estimating Malaria Vaccine Efficacy in the Absence of a Gold Standard Case Definition: Mendelian Factorial Design

References

• Athey, S., Eckles, D., and Imbens, G. W. (2018), “Exact p-Values for Network Interference,” Journal of the American Statistical Association, 113, 230–240. DOI: 10.1080/01621459.2016.1241178.
   Web of Science ®Google Scholar
• Bejon, P., Berkley, J. A., Mwangi, T., Ogada, E., Mwangi, I., Maitland, K., Williams, T., Scott, J. A. G., English, M., Lowe, B. S., and Peshu, N. (2007), “Defining Childhood Severe Falciparum Malaria for Intervention Studies,” PLoS Medicine, 4, e251. DOI: 10.1371/journal.pmed.0040251.
   PubMed Web of Science ®Google Scholar
• Bejon, P., White, M. T., Olotu, A., Bojang, K., Lusingu, J. P., Salim, N., Otsyula, N. N., Agnandji, S. T., Asante, K. P., Owusu-Agyei, S., and Abdulla, S. (2013), “Efficacy of RTS, S Malaria Vaccines: Individual-Participant Pooled Analysis of Phase 2 Data,” The Lancet Infectious Diseases, 13, 319–327. DOI: 10.1016/S1473-3099(13)70005-7.
   PubMed Web of Science ®Google Scholar
• Beneri, C., Aaron, L., Kim, S., Jean-Philippe, P., Madhi, S., Violari, A., Cotton, M. F., Mitchell, C., and Nachman, S. (2016), “Understanding NIH Clinical Case Definitions for Pediatric Intrathoracic TB by Applying Them to a Clinical Trial,” The International Journal of Tuberculosis and Lung Disease, 20, 93–100. DOI: 10.5588/ijtld.14.0848.
   PubMed Web of Science ®Google Scholar
• Berger, R. L., and Boos, D. D. (1994), “P Values Maximized Over a Confidence Set for the Nuisance Parameter,” Journal of the American Statistical Association, 89, 1012–1016.
   Web of Science ®Google Scholar
• Burgess, S., Small, D. S., and Thompson, S. G. (2017), “A Review of Instrumental Variable Estimators for Mendelian Randomization,” Statistical Methods in Medical Research, 26, 2333–2355. DOI: 10.1177/0962280215597579.
   PubMed Web of Science ®Google Scholar
• Elguero, E., Délicat-Loembet, L. M., Rougeron, V., Arnathau, C., Roche, B., Becquart, P., Gonzalez, J.-P., Nkoghe, D., Sica, L., Leroy, E. M., and Durand, P. (2015), “Malaria Continues to Select for Sickle Cell Trait in Central Africa,” Proceedings of the National Academy of Sciences of the United States of America, 112, 7051–7054. DOI: 10.1073/pnas.1505665112.
   PubMed Web of Science ®Google Scholar
• Ferreira, A., Marguti, I., Bechmann, I., Jeney, V., Chora, Â., Palha, N. R., Rebelo, S., Henri, A., Beuzard, Y., and Soares, M. P. (2011), “Sickle Hemoglobin Confers Tolerance to Plasmodium Infection,” Cell, 145, 398–409. DOI: 10.1016/j.cell.2011.03.049.
   PubMed Web of Science ®Google Scholar
• Gari, T., Loha, E., Deressa, W., Solomon, T., and Lindtjørn, B. (2018), “Malaria Increased the Risk of Stunting and Wasting Among Young Children in Ethiopia: Results of a Cohort Study,” PLOS ONE, 13, e0190983. DOI: 10.1371/journal.pone.0190983.
   PubMed Web of Science ®Google Scholar
• Genest, C., and Neslehová, J. (2007), “A Primer on Copulas for Count Data,” ASTIN Bulletin: The Journal of the IAA, 37, 475–515. DOI: 10.2143/AST.37.2.2024077.
   Web of Science ®Google Scholar
• Gong, L., Parikh, S., Rosenthal, P. J., and Greenhouse, B. (2013), “Biochemical and Immunological Mechanisms by Which Sickle Cell Trait Protects Against Malaria,” Malaria Journal, 12, 317. DOI: 10.1186/1475-2875-12-317.
   PubMed Web of Science ®Google Scholar
• Gravenor, M., and Kwiatkowski, D. (1998), “An Analysis of the Temperature Effects of Fever on the Intra-Host Population Dynamics of Plasmodium falciparum,” Parasitology, 117, 97–105. DOI: 10.1017/S0031182098002893.
   PubMed Web of Science ®Google Scholar
• Hansen, L. P. (1982), “Large Sample Properties of Generalized Method of Moments Estimators,” Econometrica: Journal of the Econometric Society, 50, 1029–1054. DOI: 10.2307/1912775.
   Web of Science ®Google Scholar
• Hayden, L. P., Cho, M. H., McDonald, M.-L. N., Crapo, J. D., Beaty, T. H., Silverman, E. K., and Hersh, C. P. (2017), “Susceptibility to Childhood Pneumonia: A Genome-Wide Analysis,” American Journal of Respiratory Cell and Molecular Biology, 56, 20–28. DOI: 10.1165/rcmb.2016-0101OC.
   PubMed Web of Science ®Google Scholar
• Hudgens, M. G., and Halloran, M. E. (2008), “Toward Causal Inference With Interference,” Journal of the American Statistical Association, 103, 832–842. DOI: 10.1198/016214508000000292.
   PubMed Web of Science ®Google Scholar
• Imbens, G. W., and Rosenbaum, P. R. (2005), “Robust, Accurate Confidence Intervals With a Weak Instrument: Quarter of Birth and Education,” Journal of the Royal Statistical Society, Series A, 168, 109–126. DOI: 10.1111/j.1467-985X.2004.00339.x.
   Web of Science ®Google Scholar
• Kang, H., Kreuels, B., Adjei, O., Krumkamp, R., May, J., and Small, D. S. (2013), “The Causal Effect of Malaria on Stunting: A Mendelian Randomization and Matching Approach,” International Journal of Epidemiology, 42, 1390–1398. DOI: 10.1093/ije/dyt116.
   PubMed Web of Science ®Google Scholar
• Kang, H., Zhang, A., Cai, T. T., and Small, D. S. (2016), “Instrumental Variables Estimation With Some Invalid Instruments and Its Application to Mendelian Randomization,” Journal of the American Statistical Association, 111, 132–144. DOI: 10.1080/01621459.2014.994705.
   Web of Science ®Google Scholar
• Kennedy, E. H. (2016), “Semiparametric Theory and Empirical Processes in Causal Inference,” in Statistical Causal Inferences and Their Applications in Public Health Research, eds. H. He, P. Wu, and D. G. Chen, Cham: Springer, pp. 141–167.
   Google Scholar
• Lachenbruch, P. A. (1998), “Sensitivity, Specificity, and Vaccine Efficacy,” Controlled Clinical Trials, 19, 569–574. DOI: 10.1016/S0197-2456(98)00042-7.
   PubMedGoogle Scholar
• Lee, K., and Small, D. S. (2019), “Estimating the Malaria Attributable Fever Fraction Accounting for Parasites Being Killed by Fever and Measurement Error,” Journal of the American Statistical Association, 114, 79–92. DOI: 10.1080/01621459.2018.1469989.
   Web of Science ®Google Scholar
• Mabunda, S., Aponte, J. J., Tiago, A., and Alonso, P. (2009), “A Country-Wide Malaria Survey in Mozambique. II. Malaria Attributable Proportion of Fever and Establishment of Malaria Case Definition in Children Across Different Epidemiological Settings,” Malaria Journal, 8, 74. DOI: 10.1186/1475-2875-8-74.
   PubMed Web of Science ®Google Scholar
• Mahmoudi, S., and Keshavarz, H. (2017), “Efficacy of Phase 3 Trial of RTS, S/AS01 Malaria Vaccine: The Need for an Alternative Development Plan,” Human Vaccines & Immunotherapeutics, 13, 2098–2101.
   PubMed Web of Science ®Google Scholar
• Marsaglia, G. (2006), “Ratios of Normal Variables,” Journal of Statistical Software, 16, 1–10. DOI: 10.18637/jss.v016.i04.
   Web of Science ®Google Scholar
• Martens, E. P., Pestman, W. R., de Boer, A., Belitser, S. V., and Klungel, O. H. (2006), “Instrumental Variables: Application and Limitations,” Epidemiology, 17, 260–267. DOI: 10.1097/01.ede.0000215160.88317.cb.
   PubMed Web of Science ®Google Scholar
• Martínez-Barricarte, R., Markle, J. G., Ma, C. S., Deenick, E. K., Ramírez-Alejo, N., Mele, F., Latorre, D., Mahdaviani, S. A., Aytekin, C., Mansouri, D., Bryant, V. L., Jabot-Hanin, F., Deswarte, C., Nieto-Patlán, A., Surace, L., Kerner, G., Itan, Y., Jovic, S., Avery, D. T., Wong, N., Rao, G., Patin, E., Okada, S., Bigio, B., Boisson, B., Rapaport, F., Seeleuthner, Y., Schmidt, M., Ikinciogullari, A., Dogu, F., Tanir, G., Tabarsi, P., Bloursaz, M. R., Joseph, J. K., Heer, A., Kong, X.-F., Migaud, M., Lazarov, T., Geissmann, F., Fleckenstein, B., Arlehamn, C. L., Sette, A., Puel, A., Emile, J.-F., van de Vosse, E., Quintana-Murci, L., Santo, J. P. D., Abel, L., Boisson-Dupuis, S., Bustamante, J., Tangye, S. G., Sallusto, F., and Casanova, J.-L. (2018), “Human IFN-γ Immunity to Mycobacteria Is Governed by Both IL-12 and IL-23,” Science Immunology, 3, eaau6759. DOI: 10.1126/sciimmunol.aau6759.
   PubMed Web of Science ®Google Scholar
• Moorthy, V. S., and Ballou, W. R. (2009), “Immunological Mechanisms Underlying Protection Mediated by RTS, S: A Review of the Available Data,” Malaria Journal, 8, 312. DOI: 10.1186/1475-2875-8-312.
   PubMed Web of Science ®Google Scholar
• Moorthy, V., Reed, Z., and Smith, P. G. (2007), “Measurement of Malaria Vaccine Efficacy in Phase III Trials: Report of a WHO Consultation,” Vaccine, 25, 5115–5123. DOI: 10.1016/j.vaccine.2007.01.085.
   PubMedGoogle Scholar
• Morton, N. (2001), “Linkage Disequilibrium,” in Encyclopedia of Genetics, eds. S. Brenner and J. H. Miller, New York: Academic Press, p. 1105.
   Google Scholar
• Ndila, C. M., Uyoga, S., Macharia, A. W., Nyutu, G., Peshu, N., Ojal, J., Shebe, M., Awuondo, K. O., Mturi, N., Tsofa, B., and Sepúlveda, N. (2018), “Human Candidate Gene Polymorphisms and Risk of Severe Malaria in Children in Kilifi, Kenya: A Case-Control Association Study,” The Lancet Haematology, 5, e333–e345. DOI: 10.1016/S2352-3026(18)30107-8.
   PubMed Web of Science ®Google Scholar
• North, T.-L., Davies, N. M., Harrison, S., Carter, A. R., Hemani, G., Sanderson, E., Tilling, K., and Howe, L. D. (2019), “Using Genetic Instruments to Estimate Interactions in Mendelian Randomization Studies,” Epidemiology, 30, e33–e35.
   PubMed Web of Science ®Google Scholar
• Olotu, A., Fegan, G., Wambua, J., Nyangweso, G., Awuondo, K. O., Leach, A., Lievens, M., Leboulleux, D., Njuguna, P., Peshu, N., and Marsh, K. (2013), “Four-Year Efficacy of RTS, S/AS01E and Its Interaction With Malaria Exposure,” New England Journal of Medicine, 368, 1111–1120. DOI: 10.1056/NEJMoa1207564.
   PubMed Web of Science ®Google Scholar
• Patel, J. C., Taylor, S. M., Meshnick, S. R., Thwai, K. L., ter Kuile, F. O., Khairallah, C., Kalilani, L., and Mwapasa, V. (2016), “Absence of Association Between Sickle Trait Hemoglobin and Placental Malaria Outcomes,” The American Journal of Tropical Medicine and Hygiene, 94, 1002–1007. DOI: 10.4269/ajtmh.15-0672.
   PubMed Web of Science ®Google Scholar
• Penny, M. A., Galactionova, K., Tarantino, M., Tanner, M., and Smith, T. A. (2015), “The Public Health Impact of Malaria Vaccine RTS, S in Malaria Endemic Africa: Country-Specific Predictions Using 18 Month Follow-Up Phase III Data and Simulation Models,” BMC Medicine, 13, 170. DOI: 10.1186/s12916-015-0408-2.
   PubMed Web of Science ®Google Scholar
• Penny, M. A., Maire, N., Studer, A., Schapira, A., and Smith, T. A. (2008), “What Should Vaccine Developers Ask? Simulation of the Effectiveness of Malaria Vaccines,” PLOS ONE, 3, e3193. DOI: 10.1371/journal.pone.0003193.
   PubMed Web of Science ®Google Scholar
• Rassen, J. A., Brookhart, M. A., Glynn, R. J., Mittleman, M. A., and Schneeweiss, S. (2009), “Instrumental Variables I: Instrumental Variables Exploit Natural Variation in Nonexperimental Data to Estimate Causal Relationships,” Journal of Clinical Epidemiology, 62, 1226–1232. DOI: 10.1016/j.jclinepi.2008.12.005.
   PubMed Web of Science ®Google Scholar
• Rees, J. M. B., Foley, C. N., and Burgess, S. (2020), “Factorial Mendelian Randomization: Using Genetic Variants to Assess Interactions,” International Journal of Epidemiology, 49, 1147–1158. DOI: 10.1093/ije/dyz161.
   PubMed Web of Science ®Google Scholar
• Regules, J. A., Cummings, J. F., and Ockenhouse, C. F. (2011), “The RTS, S Vaccine Candidate for Malaria,” Expert Review of Vaccines, 10, 589–599. DOI: 10.1586/erv.11.57.
   PubMed Web of Science ®Google Scholar
• Rosenbaum, P. R. (2002), Observational Studies, New York: Springer.
   Google Scholar
• ——— (2011), “Some Approximate Evidence Factors in Observational Studies,” Journal of the American Statistical Association, 106, 285–295.
   Web of Science ®Google Scholar
• Rosenblum, M., and van der Laan, M. J. (2009), “Using Regression Models to Analyze Randomized Trials: Asymptotically Valid Hypothesis Tests Despite Incorrectly Specified Models,” Biometrics, 65, 937–945. DOI: 10.1111/j.1541-0420.2008.01177.x.
   PubMed Web of Science ®Google Scholar
• ——— (2010), “Simple, Efficient Estimators of Treatment Effects in Randomized Trials Using Generalized Linear Models to Leverage Baseline Variables,” The International Journal of Biostatistics, 6, 13.
   Google Scholar
• Rubin, D. B. (2005), “Causal Inference Using Potential Outcomes,” Journal of the American Statistical Association, 100, 322–331. DOI: 10.1198/016214504000001880.
   Web of Science ®Google Scholar
• Russell, F. M., Reyburn, R., Chan, J., Tuivaga, E., Lim, R., Lai, J., Van, H. M. T., Choummanivong, M., Sychareun, V., Khanh, D. K. T., de Campo, M., Enarson, P., Graham, S., Vincente, S. L., Mungan, T., von Mollendorf, C., Mackenzie, G., and Mulholland, K. (2019), “Impact of the Change in WHO’s Severe Pneumonia Case Definition on Hospitalized Pneumonia Epidemiology: Case Studies From Six Countries,” Bulletin of the World Health Organization, 97, 386–393. DOI: 10.2471/BLT.18.223271.
   PubMed Web of Science ®Google Scholar
• Small, D. S., Cheng, J., and Ten Have, T. R. (2010), “Evaluating the Efficacy of a Malaria Vaccine,” The International Journal of Biostatistics, 6, 1–22. DOI: 10.2202/1557-4679.1201.
   Google Scholar
• Smith, G. D., and Ebrahim, S. (2003), “‘Mendelian Randomization’: Can Genetic Epidemiology Contribute to Understanding Environmental Determinants of Disease?,” International Journal of Epidemiology, 32, 1–22. DOI: 10.1093/ije/dyg070.
   PubMed Web of Science ®Google Scholar
• ——— (2008), “Mendelian Randomization: Genetic Variants as Instruments for Strengthening Causal Inference in Observational Studies,” in Biosocial Surveys, eds. National Research Council (US) Committee on Advances in Collecting and Utilizing Biological Indicators and Genetic Information in Social Science Surveys; M. Weinstein, J. W. Vaupel, and K. W. Wachter, Washington, DC: National Academies Press (US).
   Google Scholar
• Smith, T., Schellenberg, J. A., and Hayes, R. (1994), “Attributable Fraction Estimates and Case Definitions for Malaria in Endemic,” Statistics in Medicine, 13, 2345–2358. DOI: 10.1002/sim.4780132206.
   PubMed Web of Science ®Google Scholar
• Spiller, W., Slichter, D., Bowden, J., and Smith, G. D. (2018), “Detecting and Correcting for Bias in Mendelian Randomization Analyses Using Gene-by-Environment Interactions,” International Journal of Epidemiology, 48, 702–712. DOI: 10.1093/ije/dyy204.
   Web of Science ®Google Scholar
• Swanson, S. A., and Hernán, M. A. (2017), “The Challenging Interpretation of Instrumental Variable Estimates Under Monotonicity,” International Journal of Epidemiology, 47, 1289–1297. DOI: 10.1093/ije/dyx038.
   Web of Science ®Google Scholar
• Taylor, S. M., Parobek, C., M., and Fairhurst, R. M. (2012), “Haemoglobinopathies and the Clinical Epidemiology of Malaria: A Systematic Review and Meta-Analysis,” The Lancet Infectious Diseases, 12, 457–468. DOI: 10.1016/S1473-3099(12)70055-5.
   PubMed Web of Science ®Google Scholar
• ter Kuile, F. O., Terlouw, D. J., Kariuki, S. K., Phillips-Howard, P. A., Mirel, L. B., Hawley, W. A., Friedman, J. F., Shi, Y. P., Kolczak, M. S., Lal, A. A., and Vulule, J. M. (2003), “Impact of Permethrin-Treated Bed Nets on Malaria, Anemia, and Growth in Infants in an Area of Intense Perennial Malaria Transmission in Western Kenya,” The American Journal of Tropical Medicine and Hygiene, 68, 68–77. DOI: 10.4269/ajtmh.2003.68.68.
   PubMed Web of Science ®Google Scholar
• The RTS,S Clinical Trials Partnership (2011), “First Results of Phase 3 Trial of RTS,S/AS01 Malaria Vaccine in African Children,” New England Journal of Medicine, 365, 1863–1875.
   PubMed Web of Science ®Google Scholar
• ——— (2014), “Efficacy and Safety of the RTS,S/AS01 Malaria Vaccine During 18 Months After Vaccination: A Phase 3 Randomized, Controlled Trial in Children and Young Infants at 11 African Sites,” PLoS Medicine, 11, e1001685.
   PubMed Web of Science ®Google Scholar
• Van der Laan, M. J., and Rose, S. (2011), Targeted Learning: Causal Inference for Observational and Experimental Data, New York: Springer.
   Google Scholar
• VanderWeele, T. J., and Hernan, M. A. (2013), “Causal Inference Under Multiple Versions of Treatment,” Journal of Causal Inference, 1, 1–20. DOI: 10.1515/jci-2012-0002.
   PubMedGoogle Scholar
• Wald, A. (1940), “The Fitting of Straight Lines If Both Variables Are Subject to Error,” The Annals of Mathematical Statistics, 11, 284–300. DOI: 10.1214/aoms/1177731868.
   Google Scholar
• Williams, T. N. (2011), “How Do Hemoglobins S and C Result in Malaria Protection?,” Journal of Infectious Diseases, 204, 1651–1653. DOI: 10.1093/infdis/jir640.
   PubMed Web of Science ®Google Scholar
• Williams, T. N., Mwangi, T. W., Wambua, S., Alexander, N. D., Kortok, M., Snow, R. W., and Marsh, K. (2005), “Sickle Cell Trait and the Risk of Plasmodium falciparum Malaria and Other Childhood Diseases,” The Journal of Infectious Diseases, 192, 178–186. DOI: 10.1086/430744.
   PubMed Web of Science ®Google Scholar
• World Health Organization (2018), WHO World Malaria Report 2018, Luxembourg: World Health Organization.
   Google Scholar
• Wu, Y., Sinden, R. E., Churcher, T. S., Tsuboi, T., and Yusibov, V. (2015), “Development of Malaria Transmission-Blocking Vaccines: From Concept to Product,” in Advances in Parasitology (Vol. 89), ed. D. D. Bowman, Amsterdam: Elsevier, pp. 109–152.
   Google Scholar