What Is the Predictive Value of Animal Models for Vaccine Efficacy in Humans?: The Importance of Bridging Studies and Species-Independent Correlates of Protection
Open accessAbstract
Animal models have played a pivotal role in all stages of vaccine development.Their predictive value for vaccine effectiveness depends on the pathogen, the robustness of the animal challenge model, and the correlates of protection (if known).This article will cover key questions regarding bridging animal studies to efficacy trials in humans.Examples include human papillomavirus (HPV) vaccine in which animal protection after vaccination with heterologous prototype virus-like particles (VLPs) predicted successful efficacy trials in humans, and a recent approval of anthrax vaccine in accordance with the "Animal Rule."The establishment of animal models predictive of vaccine effectiveness in humans has been fraught with difficulties with low success rate to date.Challenges facing the use of animal models for vaccine development against Ebola and HIV will be discussed. GREAT DEBATESWhat are the most interesting topics likely to come up over dinner or drinks with your colleagues?Or, more importantly, what are the topics that don't come up because they are a little too controversial?In Immune Memory and Vaccines: Great Debates, Editors Rafi Ahmed and Shane Crotty have put together a collection of articles on such questions, written by thought leaders in these fields, with the freedom to talk about the issues as they see fit.This short, innovative format aims to bring a fresh perspective by encouraging authors to be opinionated, focus on what is most interesting and current, and avoid restating introductory material covered in many other reviews.The Editors posed 13 interesting questions critical for our understanding of vaccines and immune memory to a broad group of experts in the field.In each case, several different perspectives are provided.Note that while each author knew that there were additional scientists addressing the same question, they did not know who these authors were, which ensured the independence of the opinions and perspectives expressed in each article.Our hope is that readers enjoy these articles and that they trigger many more conversations on these important topics.
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Most drugs fail in clinical stages despite efficacy and safety in animal models.
“Most drugs fail in clinical stages (Fig. 1) despite proven efficacy and safety in animal models4,5.”
From Human disease models in drug development (2023) · cites this paper as [4]
The Concluding Remarks (page not provided) describe a low success rate in establishing animal models predictive of vaccine effectiveness, not a failure rate for drugs in clinical trials. A search for drug failures after demonstrated animal efficacy and safety found no passage addressing that claim. (LLM, conf=0.76)
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Pushko, P., Pumpens, P., & Grens, E. (2013) · Intervirology · doi:10.1159/000346773 · Cited by 5,970 · see citing works
Vaccination with ALVAC and AIDSVAX to Prevent HIV-1 Infection in Thailand
Rerks‐Ngarm, S., Pitisuttithum, P., Nitayaphan, S., Kaewkungwal, J., Chiu, J., Paris, R., Premsri, N., Namwat, C., de Souza, M. S., Adams, E. M., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0908492 · Cited by 3,036 · see citing works
Immune-Correlates Analysis of an HIV-1 Vaccine Efficacy Trial
Haynes, B. F., Gilbert, P. B., McElrath, M. J., Zolla‐Pazner, S., Tomaras, G. D., Alam, S. M., Evans, D. T., Montefiori, D. C., Karnasuta, C., Sutthent, R., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1113425 · Cited by 1,810 · see citing works
Buchbinder, S. P., Mehrotra, D. V., Duerr, A., Fitzgerald, D. W., Mogg, R., Li, D., Gilbert, P. B., Lama, J. R., Marmor, M., del Rio, C., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)61591-3 · Cited by 1,713 · see citing works
Harper, D. M., Franco, E. L., Wheeler, C. M., Ferris, D. G., Jenkins, D., Schuind, A., Zahaf, T., Innis, B. L., Naud, P., de Carvalho, N. S., et al. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17398-4 · Cited by 1,639 · see citing works
Villa, L. L., Costa, R. L. R., Petta, C. A., de Andrade, R. P., Ault, K. A., Giuliano, A. R., Wheeler, C. M., Koutsky, L. A., Malm, C., Lehtinen, M., et al. (2005) · The Lancet Oncology · doi:10.1016/s1470-2045(05)70101-7 · Cited by 1,593 · see citing works
Shiver, J. W., Fu, T., Chen, L., Casimiro, D. R., Davies, M.-E., Evans, R. K., Zhang, Z., Simon, A. J., Trigona, W. L., Dubey, S. A., et al. (2002) · Nature · doi:10.1038/415331a · Cited by 1,173 · see citing works
Restrepo, A. M. H., Longini, I. M., Egger, M., Dean, N. E., Edmunds, W. J., Camacho, A., Carroll, M. W., Doumbia, M. M., Draguez, B., Duraffour, S., et al. (2015) · The Lancet · doi:10.1016/s0140-6736(15)61117-5 · Cited by 794 · see citing works
HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case–cohort analysis
McElrath, M. J., Rosa, S. C. D., Moodie, Z., Dubey, S. A., Kierstead, L. S., Janes, H., Defawe, O., Carter, D. K., Hural, J., Akondy, R. S., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)61592-5 · Cited by 712 · see citing works
Suzich, J., Ghim, S., Palmer‐Hill, F. J., et al. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.25.11553 · Cited by 676 · see citing works
Efficacy Trial of a DNA/rAd5 HIV-1 Preventive Vaccine
Hammer, S. M., Sobieszczyk, M. E., Janes, H., Karuna, S., Mulligan, M. J., Grove, D., Koblin, B. A., Buchbinder, S., Keefer, M. C., Tomaras, G. D., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1310566 · Cited by 597 · see citing works
Breitburd, F., Kirnbauer, R., Hubbert, N. L., et al. (1995) · Journal of Virology · doi:10.1128/jvi.69.6.3959-3963.1995 · Cited by 595 · see citing works
Pathogenesis of Ebola Hemorrhagic Fever in Cynomolgus Macaques
Geisbert, T. W., Hensley, L. E., Larsen, T., Young, H. A., Reed, D. S., Geisbert, J. B., Scott, D. P., Kagan, E., Jahrling, P. B., & Davis, K. J. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63591-2 · Cited by 577 · see citing works
Evaluation of Convalescent Plasma for Ebola Virus Disease in Guinea
van Griensven, J., Edwards, T., de Lamballerie, X. N., Semple, M. G., Gallian, P., Baize, S., Horby, P., Raoul, H., Magassouba, N., Antierens, A., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1511812 · Cited by 533 · see citing works
A Randomized, Controlled Trial of ZMapp for Ebola Virus Infection
The PREVAIL II Writing Group (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1604330 · Cited by 527 · see citing works
Yates, N. L., Liao, H., Fong, Y., deCamp, A. C., Vandergrift, N., Williams, W. T., Alam, S. M., Ferrari, G., Yang, Z., Seaton, K. E., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3007730 · Cited by 449 · see citing works
Chung, A. W., Ghebremichael, M. S., Robinson, H. R., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3007736 · Cited by 410 · see citing works
A Recombinant Vesicular Stomatitis Virus Ebola Vaccine
Regules, J. A., Beigel, J. H., Paolino, K. M., Voell, J., Castellano, A. R., Hu, Z., Muñoz, P., Moon, J. E., Ruck, R. C., Bennett, J. W., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1414216 · Cited by 388 · see citing works
Dissecting polyclonal vaccine-induced humoral immunity against HIV using Systems Serology
Chung, A., Kumar, M. P., Arnold, K. B., Yu, W.-H., Schoen, M., Dunphy, L. J., Suscovich, T., Frahm, N., Linde, C., Mahan, A. E., et al. (2015) · Cell · doi:10.1016/j.cell.2015.10.027 · Cited by 360 · see citing works
Stanley, D. A., Honko, A. N., Asiedu, C. K., Trefry, J. C., Lau-Kilby, A. W., Johnson, J. C., Hensley, L. E., Ammendola, V., Abbate, A., Grazioli, F., et al. (2014) · Nature Medicine · doi:10.1038/nm.3702 · Cited by 350 · see citing works
A monovalent chimpanzee adenovirus Ebola vaccine boosted with MVA
Ewer, K., Rampling, T., Venkatraman, N., Bowyer, G., Wright, D., Lambe, T., Imoukhuede, E. B., Payne, R., Fehling, S. K., Strecker, T., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1411627 · Cited by 348 · see citing works
Pathogenesis of Ebola Hemorrhagic Fever in Primate Models
Geisbert, T. W., Young, H. A., Jahrling, P. B., et al. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63592-4 · Cited by 318 · see citing works
Virus-like Particles of Bovine Papillomavirus Type 4 in Prophylactic and Therapeutic Immunization
Kirnbauer, R., Chandrachud, L. M., O'neil, B. W., et al. (1996) · Virology · doi:10.1006/viro.1996.0220 · Cited by 317 · see citing works
Schroder, K., Irvine, K. M., Taylor, M. S., Bokil, N. J., Cao, K. L., Masterman, K., Labzin, L. I., Semple, C. A. M., Kapétanovic, R., Fairbairn, L., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110156109 · Cited by 306 · see citing works
Postexposure antibody prophylaxis protects nonhuman primates from filovirus disease
Dye, J. M., Herbert, A. S., Kuehne, A. I., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200409109 · Cited by 270 · see citing works
Zolla‐Pazner, S., deCamp, A. C., Gilbert, P. B., Williams, C. A. U., Yates, N. L., Williams, W. T., Howington, R., Fong, Y., Morris, D. E., Soderberg, K. A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087572 · Cited by 267 · see citing works
Marburg Virus Vaccines Based upon Alphavirus Replicons Protect Guinea Pigs and Nonhuman Primates
Hevey, M., Negley, D. L., Pushko, P., Smith, J., & Schmaljohn, A. L. (1998) · Virology · doi:10.1006/viro.1998.9367 · Cited by 262 · see citing works
Xiao, X., Chen, W., Feng, Y., et al. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.09.029 · Cited by 262 · see citing works
Wilson, N. A., Reed, J. S., Napoé, G. S., Piaskowski, S. M., Szymanski, A., Furlott, J. R., Gonzalez, E. J., Yant, L. J., Maness, N. J., May, G. E., et al. (2006) · Journal of Virology · doi:10.1128/jvi.00171-06 · Cited by 251 · see citing works
Evaluation in Nonhuman Primates of Vaccines against Ebola Virus
Geisbert, T. W., Pushko, P., Anderson, K., et al. (2002) · Emerging infectious diseases · doi:10.3201/eid0805.010284 · Cited by 248 · see citing works
VSV-EBOV rapidly protects macaques against infection with the 2014/15 Ebola virus outbreak strain
Marzi, A., Robertson, S. J., Haddock, E., Feldmann, F., Hanley, P. W., Scott, D. P., Strong, J. E., Kobinger, G., Best, S. M., & Feldmann, H. (2015) · Science · doi:10.1126/science.aab3920 · Cited by 241 · see citing works
Sullivan, N. J., Hensley, L. E., Asiedu, C. K., Geisbert, T. W., Stanley, D. A., Johnson, J. C., Honko, A. N., Olinger, G. G., Bailey, M., Geisbert, J. B., et al. (2011) · Nature Medicine · doi:10.1038/nm.2447 · Cited by 225 · see citing works
Geisbert, T. W., Bailey, M., Hensley, L. E., Asiedu, C. K., Geisbert, J. B., Stanley, D. A., Honko, A. N., Johnson, J. C., Mulangu, S., Pau, M. G., et al. (2011) · Journal of Virology · doi:10.1128/jvi.02407-10 · Cited by 224 · see citing works
Li, H., Wang, S., Kong, R., Ding, W., Lee, F.-H., Parker, Z., Kim, E., Learn, G. H., Hahn, P., Policicchio, B., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606636113 · Cited by 222 · see citing works
Tapia, M. D., Sow, S. O., Lyke, K. E., Haidara, F. C., Diallo, F., Doumbia, M. M., Traoré, A., Coulibaly, F., Kodio, M., Onwuchekwa, U., et al. (2015) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(15)00362-x · Cited by 219 · see citing works
Geisbert, T. W., Daddario-DiCaprio, K. M., Geisbert, J. B., et al. (2008) · Vaccine · doi:10.1016/j.vaccine.2008.09.082 · Cited by 199 · see citing works
Epidemiology of Ebola (Subtype Reston) Virus in the Philippines, 1996
Miranda, M. E., Ksiazek, T. G., Retuya, T. J. A., Khan, A. S., Sanchez, A., Fulhorst, C. F., Rollin, P. E., Calaor, A. B., MANALO, D. L., Roces, M. C., et al. (1999) · The Journal of Infectious Diseases · doi:10.1086/514314 · Cited by 197 · see citing works
Adjuvant-dependent innate and adaptive immune signatures of risk of SIVmac251 acquisition
Vaccari, M., Gordon, S. N., Fourati, S., Schifanella, L., Liyanage, N. P. M., Cameron, M. J., Keele, B. F., Shen, X., Tomaras, G. D., Billings, E., et al. (2016) · Nature Medicine · doi:10.1038/nm.4105 · Cited by 195 · see citing works
Structures of protective antibodies reveal sites of vulnerability on Ebola virus
Murin, C. D., Fusco, M. L., Bornholdt, Z. A., Qiu, X., Olinger, G. G., Zeitlin, L., Kobinger, G. P., Ward, A. B., & Saphire, E. O. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1414164111 · Cited by 183 · see citing works
Santra, S., Tomaras, G. D., Warrier, R., Nicely, N. I., Liao, H., Pollara, J., Liu, P., Alam, S. M., Zhang, R., Cocklin, S. L., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005042 · Cited by 161 · see citing works
Wong, G., Richardson, J. S., Pillet, S., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004582 · Cited by 150 · see citing works
Roels, T. H., Bloom, A. S., Buffington, J., et al. (1999) · The Journal of Infectious Diseases · doi:10.1086/514286 · Cited by 135 · see citing works
Tay, M. Z., Liu, P., Williams, L. D., McRaven, M. D., Sawant, S. S., Gurley, T. C., Xu, T. T., Dennison, S. M., Liao, H., Chenine, A., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005817 · Cited by 131 · see citing works
Chowell, G., Viboud, C. G., Hyman, J. M., & Simonsen, L. (2014) · PLoS Currents · doi:10.1371/currents.outbreaks.8b55f4bad99ac5c5db3663e916803261 · Cited by 111 · see citing works
Establishing Efficacy of Human Products Using Animals
Snoy, P. (2010) · Veterinary Pathology · doi:10.1177/0300985810372506 · Cited by 109 · see citing works
Vesicular Stomatitis Virus–based Vaccines against Lassa and Ebola Viruses
Marzi, A., Feldmann, F., Geisbert, T. W., et al. (2014) · Emerging infectious diseases · doi:10.3201/eid2102.141649 · Cited by 98 · see citing works
Pathology of Experimental Aerosol Zaire Ebolavirus Infection in Rhesus Macaques
Twenhafel, N. A., Mattix, M. E., Johnson, J. C., Robinson, C. G., Pratt, W. D., Cashman, K. A., Wahl‐Jensen, V., Terry, C., Olinger, G. G., Hensley, L. E., et al. (2012) · Veterinary Pathology · doi:10.1177/0300985812469636 · Cited by 98 · see citing works
van Griensven, J., Weggheleire, A. D., Délamou, A., Smith, P. G., Edwards, T., Vandekerckhove, P. G., Bah, E. I., Colebunders, R., Isola, H., Lazaygues, C., et al. (2015) · Clinical Infectious Diseases · doi:10.1093/cid/civ680 · Cited by 94 · see citing works
Ebola Hemorrhagic Fever, Democratic Republic of the Congo, 1995: Determinants of Survival
Sadek, R., Khan, A. S., Stevens, G., et al. (1999) · The Journal of Infectious Diseases · doi:10.1086/514311 · Cited by 91 · see citing works
Delayed Disease Progression in Cynomolgus Macaques Infected with Ebola Virus Makona Strain
Marzi, A., Feldmann, F., Hanley, P. W., Scott, D. P., Günther, S., & Feldmann, H. (2015) · Emerging infectious diseases · doi:10.3201/eid2110.150259 · Cited by 88 · see citing works
Immune Activation with HIV Vaccines
Fauci, A. S., Marovich, M., Dieffenbach, C. W., Hunter, E., & Buchbinder, S. (2014) · Science · doi:10.1126/science.1250672 · Cited by 78 · see citing works
Fera, D., Schmidt, A. G., Haynes, B. F., Gao, F., Liao, H., Kepler, T. B., & Harrison, S. C. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409954111 · Cited by 71 · see citing works
Maturation Pathways of Cross-Reactive HIV-1 Neutralizing Antibodies
Xiao, X., Chen, W., Feng, Y., et al. (2009) · Viruses · doi:10.3390/v1030802 · Cited by 69 · see citing works
Dugast, A., Chan, Y. N., Hoffner, M., Licht, A. F., Nkolola, J. P., Li, H., Streeck, H., Suscovich, T. J., Ghebremichael, M. S., Ackerman, M. E., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097229 · Cited by 65 · see citing works
Evaluation of Immunogenicity and Efficacy of Anthrax Vaccine Adsorbed for Postexposure Prophylaxis
Ionin, B. I., Hopkins, R. J., Pleune, B., et al. (2013) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00099-13 · Cited by 64 · see citing works
Animal models in HIV-1 protection and therapy
Hessell, A. J., & Haigwood, N. L. (2015) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0000000000000152 · Cited by 56 · see citing works
HIV-1 vaccine immunogen design strategies
Mann, J. K., & Ndung’u, T. (2015) · Virology Journal · doi:10.1186/s12985-014-0221-0 · Cited by 50 · see citing works
IgG Binding Characteristics of Rhesus Macaque FcγR
Chan, Y. N., Boesch, A. W., Osei‐Owusu, N. Y., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502252 · Cited by 50 · see citing works
Selection of Unadapted, Pathogenic SHIVs Encoding Newly Transmitted HIV-1 Envelope Proteins
Prete, G. Q. D., Eilers, B., Moldt, B., Keele, B. F., Estes, J. D., Rodriguez, A. B., Sampias, M., Oswald, K. A., Fast, R. L., Trubey, C. M., et al. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.08.003 · Cited by 48 · see citing works
Marburg and Ebola virus infections in laboratory non-human primates: a literature review.
Schou, S., & Hansen, A. K. (2000) · PubMed · Cited by 44 · see citing works
Characterizing Ebola Transmission Patterns Based on Internet News Reports
Cleaton, J. M., Viboud, C. G., Simonsen, L., Hurtado, A. M., & Chowell, G. (2015) · Clinical Infectious Diseases · doi:10.1093/cid/civ748 · Cited by 44 · see citing works
Boyd, D. F., Peterson, D., Haggarty, B., Jordan, A. P. O., Hogan, M. J., Goo, L., Hoxie, J. A., & Overbaugh, J. M. (2014) · Journal of Virology · doi:10.1128/jvi.02680-14 · Cited by 44 · see citing works
Nonhuman primate models for the evaluation of HIV-1 preventive vaccine strategies
Prete, G. Q. D., Lifson, J. D., & Keele, B. F. (2016) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0000000000000311 · Cited by 42 · see citing works
Licensure of vaccines using the Animal Rule
Burns, D. (2012) · Current Opinion in Virology · doi:10.1016/j.coviro.2012.01.004 · Cited by 39 · see citing works
The modern era of HIV-1 vaccine development
Mascola, J. R. (2015) · Science · doi:10.1126/science.aac7800 · Cited by 37 · see citing works
Bett, A. J., Dubey, S. A., Mehrotra, D. V., Guan, L., Long, R. S., Anderson, K., Collins, K., Gaunt, C., Fernandez, R., Cole, S., et al. (2010) · Vaccine · doi:10.1016/j.vaccine.2010.09.079 · Cited by 31 · see citing works
Brody, I. B., Calcedo, R., Roy, S., Carnathan, D. G., Grant, R. L., Qin, Q., Boyd, S., Ratcliffe, S. J., Veeder, C. L., Bellamy, S. L., et al. (2014) · Journal of Virology · doi:10.1128/jvi.03850-13 · Cited by 31 · see citing works
Asmal, M., Luedemann, C., Lavine, C. L., et al. (2014) · Virology · doi:10.1016/j.virol.2014.10.032 · Cited by 29 · see citing works
Peters, C. J., & Khan, A. S. (1999) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-59949-1_6 · Cited by 28 · see citing works
TLR7/8 agonists activate a mild immune response in rabbits through TLR8 but not TLR7
Lai, C.-Y., Liu, Y., Yu, G., et al. (2014) · Vaccine · doi:10.1016/j.vaccine.2014.07.104 · Cited by 23 · see citing works
Development of SHIV s with circulating, transmitted HIV ‐1 variants
Sharma, A., Boyd, D. F., & Overbaugh, J. M. (2015) · Journal of Medical Primatology · doi:10.1111/jmp.12179 · Cited by 22 · see citing works
Lopker, M. J., Prete, G. Q. D., Estes, J. D., et al. (2016) · Journal of Virology · doi:10.1128/jvi.00718-16 · Cited by 22 · see citing works
Immunology of protection from Ebola virus infection
Krause, P. R., Bryant, P. R., Clark, T. A., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa8202 · Cited by 20 · see citing works
Sholukh, A. M., Siddappa, N. B., Shanmuganathan, V., et al. (2014) · Retrovirology · doi:10.1186/1742-4690-11-8 · Cited by 15 · see citing works
Approaches to demonstration of Ebola virus vaccine efficacy
Krause, P. R., Cavaleri, M., Coleman, G., et al. (2015) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(15)00027-4 · Cited by 13 · see citing works
Ebola vaccine trials: a race against the clock
Chowell, G., & Viboud, C. G. (2015) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(15)70159-3 · Cited by 11 · see citing works
Yuan, T., Li, J., Zhang, Y., Wang, Y., Streaker, E. D., Dimitrov, D. S., & Zhang, M.-Y. (2011) · Vaccine · doi:10.1016/j.vaccine.2011.07.046 · Cited by 10 · see citing works
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Human organs-on-chips for disease modelling, drug development and personalized medicine
Ingber, D. E. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00466-9 · Cited by 1,589 · see citing works
Human disease models in drug development
Loewa, A., Feng, J. J., & Hedtrich, S. (2023) · Nature Reviews Bioengineering · doi:10.1038/s44222-023-00063-3 · Cited by 331 · see citing works
- Authors
- Golding, H., Khurana, S., & Zaitseva, M.
- Affiliations
- Center for Biologics Evaluation and Research (US)
- Venue
- Cold Spring Harbor Perspectives in Biology
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2017-03-27
- Volume
- 10
- Issue
- 4
- Pages
- a028902
- ISSN
- 1943-0264 (ISSN-L)
- PMC
- PMC5880166
- OpenAlex
- W2601086746
- Cited by
- 67
- References
- 77
- Citations by year
- 2026: 10 · 2025: 14 · 2024: 9 · 2023: 9 · 2022: 7 · 2021: 8 · 2020: 5 · 2019: 3 · 2018: 2
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cold Spring Harbor Perspectives in Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Veterinary › Small Animals › Animal testing and alternatives
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Immunology and Microbiology › Virology › Poxvirus research and outbreaks
- Keywords
- animal models, vaccine efficacy, predictive value, correlates of protection, HPV vaccine, virus-like particles, anthrax vaccine, Animal Rule, Ebola vaccine, HIV vaccine, immunological memory
- MeSH terms
- Proof of Concept Study, Animals, Anthrax, Disease Models, Animal, Drug Evaluation, Preclinical, Humans, Species Specificity, Vaccines, AIDS Vaccines, Drug Approval, Anthrax Vaccines, Papillomaviridae, Ebola Vaccines, Papillomavirus Vaccines
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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