Trials and tribulations on the path to developing a dengue vaccine

Vaccine

Volumn 33, Issue , 2015, Pages D24-D31

  Thomas, Stephen J ^a   Rothman, Alan L ^b  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

Dengue; Immunology; Vaccine

Indexed keywords

DENGUE VACCINE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

CLINICAL EFFECTIVENESS; CLINICAL TRIAL (TOPIC); DENGUE; DRUG SAFETY; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; VECTOR CONTROL; ANIMAL; BLOOD; DENGUE VIRUS; DISEASE MODEL; DRUG DEVELOPMENT; IMMUNOLOGY; MEDICAL RESEARCH; MOUSE;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BIOMEDICAL RESEARCH; CLINICAL TRIALS AS TOPIC; DENGUE; DENGUE VACCINES; DENGUE VIRUS; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; HUMANS; MICE;

EID: 84951569672     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.05.095     Document Type: Review

References (137)

1. Bhatt S., et al. The global distribution and burden of dengue. Nature 2013, 496:504-507.
2. Endy T.P., et al. Epidemiology of inapparent and symptomatic acute dengue virus infection: a prospective study of primary school children in kamphaeng phet, Thailand. Am J Epidemiol 2002, 156(1):40-51.
3. Yoon I.K., et al. Underrecognized mildly symptomatic viremic dengue virus infections in rural Thai schools and villages. J Infect Dis 2012, 206(3):389-398.
4. Anderson K.B., et al. Burden of symptomatic dengue infection in children at primary school in Thailand: a prospective study. Lancet 2007, 369(9571):1452-1459.
5. Sabin A.B. Research on dengue during World War II. Am J Trop Med Hyg 1952, 1:30-50.
6. Burke D.S., et al. A prospective study of dengue infections in Bangkok. Am J Trop Med Hyg 1988, 38(1):172-180.
7. Anderson K.B., et al. A shorter time interval between first and second dengue infections is associated with protection from clinical illness in a school-based cohort in Thailand. J Infect Dis 2014, 209:360-368.
8. Gibbons R.V., et al. Analysis of repeat hospital admissions for dengue to estimate the frequency of third or fourth dengue infections resulting in admissions and dengue hemorrhagic fever: and serotype sequences. Am J Trop Med Hyg 2007, 77(5):910-913.
9. Heinz F.X., Allison S.L. Flavivirus structure and membrane fusion. Adv Virus Res 2003, 59:63-97.
10. Thomas S.J. Developing a dengue vaccine: progress and future challenges. Ann NY Acad Sci 2014, 1323:140-159.
11. Shresta S., et al. Early activation of natural killer and B cells in response to primary dengue virus infection in A/J mice. Virology 2004, 319(2):262-273.
12. Verma R., Sahu R., Holla V. Neurological manifestations of dengue infection: a review. J Neurol Sci 2014, 346(1-2):26-34.
13. Solomon T., et al. Neurological manifestations of dengue infection. Lancet 2000, 355(9209):1053-1059.
14. Johnson A.J., Roehrig J.T. New mouse model for dengue virus vaccine testing. J Virol 1999, 73(1):783-786.
15. Zellweger R.M., Shresta S. Mouse models to study dengue virus immunology and pathogenesis. Front Immunol 2014, 5:151.
16. Zellweger R.M., Prestwood T.R., Shresta S. Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 2010, 7(2):128-139.
17. An J., et al. Development of a novel mouse model for dengue virus infection. Virology 1999, 263(1):70-77.
18. Wu S.J., et al. Evaluation of the severe combined immunodeficient (SCID) mouse as an animal model for dengue viral infection. Am J Trop Med Hyg 1995, 52(5):468-476.
19. Bente D.A., et al. Dengue fever in humanized NOD/SCID mice. J Virol 2005, 79(21):13797-13799.
20. Kuruvilla J.G., et al. Dengue virus infection and immune response in humanized RAG2(-/-)gamma(c)(-/-) (RAG-hu) mice. Virology 2007, 369(1):143-152.
21. Mota J., Rico-Hesse R. Humanized mice show clinical signs of dengue fever according to infecting virus genotype. J Virol 2009, 83(17):8638-8645.
22. Jaiswal S., et al. Dengue virus infection and virus-specific HLA-A2 restricted immune responses in humanized NOD-scid IL2rgammanull mice. PLoS ONE 2009, 4(10):e7251.
23. Frias-Staheli N., et al. Utility of humanized BLT mice for analysis of dengue virus infection and antiviral drug testing. J Virol 2014, 88(4):2205-2218.
24. Rosen L. Experimental infection of New World monkeys with dengue and yellow fever viruses. Am J Trop Med Hyg 1958, 7(4):406-410.
25. Halstead S.B., Shotwell H., Casals J. Studies on the pathogenesis of dengue infection in monkeys. I. Clinical laboratory responses to primary infection. J Infect Dis 1973, 128(1):7-14.
26. Halstead S.B., Shotwell H., Casals J. Studies on the pathogenesis of dengue infection in monkeys. II. Clinical laboratory responses to heterologous infection. J Infect Dis 1973, 128(1):15-22.
27. Clark K.B., et al. Can non-human primates serve as models for investigating dengue disease pathogenesis?. Front Microbiol 2013, 4:305.
28. Sariol C.A., White L.J. Utility, limitations, and future of non-human primates for dengue research and vaccine development. Front Immunol 2014, 5:452.
29. Koraka P., et al. Characterization of humoral and cellular immune responses in cynomolgus macaques upon primary and subsequent heterologous infections with dengue viruses. Microb Infect 2007, 9(8):940-946.
30. Althouse B.M., et al. Viral kinetics of primary dengue virus infection in non-human primates: a systematic review and individual pooled analysis. Virology 2014, 452-453:237-246.
31. Onlamoon N., et al. Dengue virus-induced hemorrhage in a nonhuman primate model. Blood 2010, 115(9):1823-1834.
32. Goncalvez A.P., et al. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 2007, 104(22):9422-9427.
33. Robert Putnak J., et al. An evaluation of dengue type-2 inactivated: recombinant subunit, and live-attenuated vaccine candidates in the rhesus macaque model. Vaccine 2005, 23(35):4442-4452.
34. Osorio J.E., et al. Efficacy of a tetravalent chimeric dengue vaccine (DENVax) in cynomolgus macaques. Am J Trop Med Hyg 2011, 84(6):978-987.
35. Rice C.M., et al. Transcription of infectious yellow fever RNA from full-length cDNA templates produced by in vitro ligation. New Biol 1989, 1(3):285-296.
36. Chambers T.J., et al. Yellow fever/Japanese encephalitis chimeric viruses: construction and biological properties. J Virol 1999, 73(4):3095-3101.
37. Guirakhoo F., et al. Recombinant chimeric yellow fever-dengue type 2 virus is immunogenic and protective in nonhuman primates. J Virol 2000, 74(12):5477-5485.
38. Lai C.J., Monath T.P. Chimeric flaviviruses: novel vaccines against dengue fever, tick-borne encephalitis, and Japanese encephalitis. Adv Virus Res 2003, 61:469-509.
39. Guirakhoo F., et al. Construction: safety, and immunogenicity in nonhuman primates of a chimeric yellow fever-dengue virus tetravalent vaccine. J Virol 2001, 75(16):7290-7304.
40. Sabchareon A., et al. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 2012, 380(9853):1559-1567.
41. Capeding M.R., et al. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet 2014, 384(9951):1358-1365.
42. Villar L., et al. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 2015, 372(2):113-123.
43. Thomas S.J. Preventing dengue-is the possibility now a reality?. N Engl J Med 2015, 372(2):172-173.
44. Kinney R.M., et al. Construction of infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 1997, 230(2):300-308.
45. Huang C.Y., et al. Chimeric dengue type 2 (vaccine strain PDK-53)/dengue type 1 virus as a potential candidate dengue type 1 virus vaccine. J Virol 2000, 74(7):3020-3028.
46. Butrapet S., et al. Attenuation markers of a candidate dengue type 2 vaccine virus: strain 16681 (PDK-53), are defined by mutations in the 5' noncoding region and nonstructural proteins 1 and 3. J Virol 2000, 74(7):3011-3019.
47. Huang C.Y., et al. Dengue 2 PDK-53 virus as a chimeric carrier for tetravalent dengue vaccine development. J Virol 2003, 77(21):11436-11447.
48. Butrapet S., Kinney R.M., Huang C.Y. Determining genetic stabilities of chimeric dengue vaccine candidates based on dengue 2 PDK-53 virus by sequencing and quantitative TaqMAMA. J Virol Methods 2006, 131(1):1-9.
49. Huang C.Y., et al. Genetic and phenotypic characterization of manufacturing seeds for a tetravalent dengue vaccine (DENVax). PLoS Negl Trop Dis 2013, 7(5):e2243.
50. Osorio J.E., et al. Development of DENVax: a chimeric dengue-2 PDK-53-based tetravalent vaccine for protection against dengue fever. Vaccine 2011, 29(42):7251-7260.
51. Gordon G.S., et al. A phase 2 age-de-escalation clinical trial of a recombinant live attenuated tetravalent dengue vaccine (DENVax) in healthy volunteers from endemic countries. American society of tropical medicine and hygiene annual meeting 2013.
52. Gordon G.S., et al. Effect of formulation ratios and dosing schedules on the safety and immunogenicity of a recombinant live attenuated tetravalent dengue vaccine (DENVax) in healthy adult volunteers. American society of tropical medicine and hygiene annual meeting 2013.
53. Osorio J.E., et al. Safety and immunogenicity of a recombinant live attenuated tetravalent dengue vaccine (DENVax) in flavivirus-naive healthy adults in Colombia: a randomised, placebo-controlled, phase 1 study. Lancet Infect Dis 2014, 14(9):830-838.
54. Blaney J.E., et al. Chemical mutagenesis of dengue virus type 4 yields mutant viruses which are temperature sensitive in vero cells or human liver cells and attenuated in mice. J Virol 2001, 75(20):9731-9740.
55. Lai C.J., et al. Infectious RNA transcribed from stably cloned full-length cDNA of dengue type 4 virus. Proc Natl Acad Sci USA 1991, 88(12):5139-5143.
56. Bray M., Lai C.J. Dengue virus premembrane and membrane proteins elicit a protective immune response. Virology 1991, 185(1):505-508.
57. Men R., et al. Dengue type 4 virus mutants containing deletions in the 3' noncoding region of the RNA genome: analysis of growth restriction in cell culture and altered viremia pattern and immunogenicity in rhesus monkeys. J Virol 1996, 70(6):3930-3937.
58. Durbin A.P., et al. rDEN4delta30: a live attenuated dengue virus type 4 vaccine candidate, is safe, immunogenic, and highly infectious in healthy adult volunteers. J Infect Dis 2005, 191(5):710-718.
59. Blaney J.E., et al. Development of a live attenuated dengue virus vaccine using reverse genetics. Viral Immunol 2006, 19(1):10-32.
60. McArthur J.H., et al. Phase I clinical evaluation of rDEN4Delta30-200,201: a live attenuated dengue 4 vaccine candidate designed for decreased hepatotoxicity. Am J Trop Med Hyg 2008, 79(5):678-684.
61. Durbin A.P., et al. The live attenuated dengue serotype 1 vaccine rDEN1Delta30 is safe and highly immunogenic in healthy adult volunteers. Hum Vaccines 2006, 2(4):167-173.
62. Durbin A.P., et al. rDEN2/4Delta30(ME): a live attenuated chimeric dengue serotype 2 vaccine is safe and highly immunogenic in healthy dengue-naive adults. Hum Vaccines 2006, 2(6):255-260.
63. Durbin A.P., et al. Development and clinical evaluation of multiple investigational monovalent DENV vaccines to identify components for inclusion in a live attenuated tetravalent DENV vaccine. Vaccine 2011, 29(42):7242-7250.
64. Durbin A.P., et al. Heterotypic dengue infection with live attenuated monotypic dengue virus vaccines: implications for vaccination of populations in areas where dengue is endemic. J Infect Dis 2011, 203(3):327-334.
65. Durbin A.P., et al. A single dose of the DENV-1 candidate vaccine rDEN1Delta30 is strongly immunogenic and induces resistance to a second dose in a randomized trial. PLoS Negl Trop Dis 2011, 5(8):e1267.
66. Durbin A.P., et al. A single dose of any of four different live attenuated tetravalent dengue vaccines is safe and immunogenic in flavivirus-naive adults: a randomized, double-blind clinical trial. J Infect Dis 2013, 207(6):957-965.
67. Lindow J.C., et al. Vaccination of volunteers with low-dose: live-attenuated, dengue viruses leads to serotype-specific immunologic and virologic profiles. Vaccine 2013, 31(33):3347-3352.
68. Durbin A.P., et al. The live attenuated tetravalent dengue candidate vaccine TV003 is well tolerated and highly immunogenic in flavivirus-experienced subjects. American society of tropical medicine and hygiene annual meeting 2013.
69. Sabin A.B. Recent advances in our knowledge of dengue and sandfly fever. Am J Trop Med Hyg 1955, 4(2):198-207.
70. Innis B.L., et al. Virulence of a live dengue virus vaccine candidate: a possible new marker of dengue virus attenuation. J Infect Dis 1988, 158(4):876-880.
71. McKee K.T., et al. Lack of attenuation of a candidate dengue 1 vaccine (45AZ5) in human volunteers. Am J Trop Med Hyg 1987, 36(2):435-442.
72. Hoke C.H., et al. Preparation of an attenuated dengue 4 (341750 Carib) virus vaccine. II. Safety and immunogenicity in humans. Am J Trop Med Hyg 1990, 43(2):219-226.
73. Edelman R., et al. A live attenuated dengue-1 vaccine candidate (45AZ5) passaged in primary dog kidney cell culture is attenuated and immunogenic for humans. J Infect Dis 1994, 170(6):1448-1455.
74. Edelman R., et al. Phase I trial of 16 formulations of a tetravalent live-attenuated dengue vaccine. Am J Trop Med Hyg 2003, 69(6 Suppl):48-60.
75. Kanesa-Thasan N., et al. Phase 1 studies of Walter Reed Army Institute of Research candidate attenuated dengue vaccines: selection of safe and immunogenic monovalent vaccines. Am J Trop Med Hyg 2003, 69(6 Suppl):17-23.
76. Sun W., et al. Vaccination of human volunteers with monovalent and tetravalent live-attenuated dengue vaccine candidates. Am J Trop Med Hyg 2003, 69(6 Suppl):24-31.
77. Sun W., et al. Phase 2 clinical trial of three formulations of tetravalent live-attenuated dengue vaccine in flavivirus-naive adults. Hum Vaccines 2009, 5(1):33-40.
78. Watanaveeradej V., et al. Safety and immunogenicity of a tetravalent live-attenuated dengue vaccine in flavivirus-naive infants. Am J Trop Med Hyg 2011, 85(2):341-351.
79. Simasathien S., et al. Safety and immunogenicity of a tetravalent live-attenuated dengue vaccine in flavivirus naive children. Am J Trop Med Hyg 2008, 78(3):426-433.
80. Thomas S.J., et al. A phase II: randomized, safety and immunogenicity study of a re-derived, live-attenuated dengue virus vaccine in healthy adults. Am J Trop Med Hyg 2013, 88(1):73-88.
81. Watanaveeradej V., et al. Safety and immunogenicity of a rederived, live-attenuated dengue virus vaccine in healthy adults living in Thailand: a randomized trial. Am J Trop Med Hyg 2014, 91(1):119-128.
82. Putnak R., et al. Development of a purified, inactivated, dengue-2 virus vaccine prototype in Vero cells: immunogenicity and protection in mice and rhesus monkeys. J Infect Dis 1996, 174(6):1176-1184.
83. Putnak R., et al. Immunogenic and protective response in mice immunized with a purified: inactivated, Dengue-2 virus vaccine prototype made in fetal rhesus lung cells. Am J Trop Med Hyg 1996, 55(5):504-510.
84. Eckels K.H., Putnak R. Formalin-inactivated whole virus and recombinant subunit flavivirus vaccines. Adv Virus Res 2003, 61:395-418.
85. Schmidt A., et al. Phase 1 study of a tetravalent dengue purified inactivated virus (DPIV) vaccine in healthy U.S. adults. American society of tropical medicine and hygiene annual meeting 2013.
86. Coller B.A., et al. The development of recombinant subunit envelope-based vaccines to protect against dengue virus induced disease. Vaccine 2011, 29(42):7267-7275.
87. Clements D.E., et al. Development of a recombinant tetravalent dengue virus vaccine: immunogenicity and efficacy studies in mice and monkeys. Vaccine 2010, 28(15):2705-2715.
88. Beckett C.G., et al. Evaluation of a prototype dengue-1 DNA vaccine in a Phase 1 clinical trial. Vaccine 2011, 29(5):960-968.
89. Raviprakash K., et al. A dengue DNA vaccine formulated with Vaxfectin ((R)) is well tolerated, and elicits strong neutralizing antibody responses to all four dengue serotypes in New Zealand white rabbits. Hum Vaccines Immunother 2012, 8:1764-1768.
90. Edelman R., Hombach J. Guidelines for the clinical evaluation of dengue vaccines in endemic areas: summary of a World Health Organization technical consultation. Vaccine 2008, 26(33):4113-4119.
91. Villar L., et al. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 2015, 372(2):113-123.
92. Vaughn D.W., et al. Dengue viremia titer: antibody response pattern and virus serotype correlate with disease severity. J Infect Dis 2000, 181(1):2-9.
93. Mammen M.P., et al. Spatial and temporal clustering of dengue virus transmission in Thai villages. PLoS Med 2008, 5(11):e205.
94. Yoon I.K., et al. Fine scale spatiotemporal clustering of dengue virus transmission in children and Aedes aegypti in rural Thai villages. PLoS Negl Trop Dis 2012, 6(7):e1730.
95. Endy T.P., et al. Determinants of inapparent and symptomatic dengue infection in a prospective study of primary school children in Kamphaeng Phet, Thailand. PLoS Negl Trop Dis 2011, 5(3):e975.
96. Wahala W.M., et al. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog 2010, 6(3):e1000821.
97. Endy T.P., et al. Relationship of pre-existing dengue virus (DV) neutralizing antibody levels to viremia and disease severity in a prospective cohort study of DV infection in Thailand. J Infect Dis 2004, 189(6):990-1000.
98. Buddhari D., et al. Dengue virus neutralizing antibody levels associated with protection from infection in thai cluster studies. PLoS Negl Trop Dis 2014, 8(10):e3230.
99. Salje H., et al. Variability in dengue titer estimates from plaque reduction neutralization tests poses a challenge to epidemiological studies and vaccine development. PLoS Negl Trop Dis 2014, 8(6):e2952.
100. Thomas S.J., et al. Dengue plaque reduction neutralization test (PRNT) in primary and secondary dengue virus infections: How alterations in assay conditions impact performance. Am J Trop Med Hyg 2009, 81(5):825-833.
101. de Alwis R., et al. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad Sci USA 2012, 109(19):7439-7444.
102. Laoprasopwattana K., et al. Dengue Virus (DV) enhancing antibody activity in preillness plasma does not predict subsequent disease severity or viremia in secondary DV infection. J Infect Dis 2005, 192(3):510-519.
103. Moi M.L., et al. Discrepancy in dengue virus neutralizing antibody titers between plaque reduction neutralizing tests with Fcgamma receptor (FcgammaR)-negative and FcgammaR-expressing BHK-21 cells. Clin Vaccine Immunol 2010, 17(3):402-407.
104. Rothman A.L. Dengue: defining protective versus pathologic immunity. J Clin Invest 2004, 113(7):946-951.
105. Mangada M.M., et al. Dengue-specific T cell responses in peripheral blood mononuclear cells obtained prior to secondary dengue virus infections in Thai schoolchildren. JID 2002, 185(12):1697-1703.
106. Hatch S., et al. Intracellular cytokine production by dengue virus-specific T cells correlates with subclinical secondary infection. J Infect Dis 2011, 203:1282-1291.
107. Haynes B.F., et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012, 366(14):1275-1286.
108. Ewer K.J., et al. Protective CD8+ T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat Commun 2013, 4:2836.
109. Rothman A.L. Cellular immunology of sequential dengue virus infection and its role in disease pathogenesis. Curr Top Microbiol Immunol 2010, 338:83-98.
110. Anderson K.B., et al. Preexisting Japanese encephalitis virus neutralizing antibodies and increased symptomatic dengue illness in a school-based cohort in Thailand. PLoS Negl Trop Dis 2011, 5(10):e1311.
111. Hoke C.H., et al. Protection against Japanese encephalitis by inactivated vaccines. N Engl J Med 1988, 319(10):608-614.
112. Yauch L.E., Shresta S. Mouse models of dengue virus infection and disease. Antiviral Res 2008, 80(2):87-93.
113. Moser J.M., et al. Optimization of a dendritic cell-based assay for the in vitro priming of naive human CD4+ T cells. J Immunol Methods 2010, 353(1-2):8-19.
114. Kirby A.E., Teunis P.F., Moe C.L. Two human challenge studies confirm high infectivity of norwalk virus. J Infect Dis 2015, 211(1):166-167.
115. Jones C., Darton T.C., Pollard A.J. Why the development of effective typhoid control measures requires the use of human challenge studies. Front Microbiol 2014, 5:707.
116. Killingley B., et al. Use of a human influenza challenge model to assess person-to-person transmission: proof-of-concept study. J Infect Dis 2012, 205(1):35-43.
117. Killingley B., et al. Potential role of human challenge studies for investigation of influenza transmission. Lancet Infect Dis 2011, 11(11):879-886.
118. Spring M., Polhemus M., Ockenhouse C. Controlled human malaria infection. J Infect Dis 2014, 209(Suppl 2):S40-S45.
119. Miller F.G., Grady C. The ethical challenge of infection-inducing challenge experiments. Clin Infect Dis 2001, 33(7):1028-1033.
120. Hope T., McMillan J. Challenge studies of human volunteers: ethical issues. J Med Ethics 2004, 30(1):110-116.
121. Kotloff K.L. Human challenge studies with infectious agents. J Investig Med 2003, 51(Suppl. 1):S6-S11.
122. Graham H. Dengue: a study of its mode of propagation and pathology. Med Rec NY 1902, 61:204-207.
123. Graham H. The dengue: a study of its pathology and mode of propagation. J Trop Med 1902, 61:204-207.
124. Ashburn P.M., Craig C.F. Experimental investigations regarding the etiology of dengue fever. J Infect Dis 1907, 4:440-475.
125. Siler J.F., Hall M.W., Hitchens A.P. Dengue: its history, epidemilogy, mechanism of transmission, etiology, clinical manifestations, immunity, and prevention. Philippine J Sci 1926, 29:1-304.
126. Cleland J.B., Bradley B., Macdonald W. Further experiments in the etiology of dengue fever. J Hyg (Lond) 1919, 18(3):217-254.
127. Simmons J.S., St John J.H., Reynolds F.H.K. Experimental studies of dengue. Philippine J Sci 1931, 44:1-252.
128. Sawada T., Sato H., Sai S. On the experimental dengue infection in man. Nippon Igaku 1943, 3325:529-531.
129. Sabin A.B., Schlesinger R.W. Production of immunity to dengue with virus modified by propagation in mice. Science 1945, 101(2634):640-642.
130. McCoy O.R., Sabin A.B. Dengue, in Preventive Medicine in World War II. Communicable Diseases. Arthropodborne Diseases Other Than Malaria 1946, 29-62. Office of the Surgeon General, Washington, DC. J.B. Coates, E.C. Hoff, P.M. Hoff (Eds.).
131. Hotta S. Experimental studies in dengue I. Isolation, identification and modification of the virus. J Infect Dis 1952, 90(1):1-9.
132. Yaoi H. A summary of our studies on dengue. Yokohama Med Bull 1958, 9(1):1-20.
133. Cassetti M.C., Thomas S.J. Dengue human infection model: introduction. J Infect Dis 2014, 209(Suppl. 2):S37-S39.
134. Endy T.P. Dengue human infection model performance parameters. J Infect Dis 2014, 209(Suppl. 2):S56-S60.
135. Mores C.N., Christofferson R.C., Davidson S.A. The role of the mosquito in a dengue human infection model. J Infect Dis 2014, 209(Suppl. 2):S71-S78.
136. Rothman A.L. DHIM supporting immunologic investigations and the identification of immune correlates of protection. J Infect Dis 2014, 209(Suppl. 2):S61-S65.
137. Whitehorn J., Van V.C., Simmons C.P. Dengue human infection models supporting drug development. J Infect Dis 2014, 209(Suppl. 2):S66-S70.