1921
Volume 87, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Secondary heterologous dengue infection is a risk factor for severe disease manifestations because of the immune-enhancement phenomenon. Succeeding clinical infections are seldom reported, and the clinical course of tertiary and quaternary dengue infections is not clear. Cuba represents a unique environment to study tertiary/quaternary dengue infections in a population with known clinical and serologic dengue markers and no dengue endemicity. We took advantage of this exceptional epidemiologic condition to study the effect of primary, secondary, tertiary, and quaternary dengue infection exposure on the expression of pro-inflammatory and regulatory cytokines, critical in dengue infection pathogenesis, by using a dengue infection model. Whereas secondary exposure induced a high cytokine response, we found a significantly lower expression of tumor necrosis factor-α, interferon-γ, interleukin-10, and tumor growth factor-β after tertiary and quaternary infectious challenge. Significant differences in expression of the cytokines were seen between the dengue immune profiles, suggesting that the sequence in which the immune system encounters serotypes may be important in determining the nature of the immune response to subsequent infections.

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2012-09-05
2017-11-21
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References

  1. Guha-Sapir D, Schimmer B, , 2005. Dengue fever: new paradigms for a changing epidemiology. Emerg Themes Epidemiol 2: 1.[Crossref]
  2. Halstead SB, , 2007. Dengue. Lancet 370: 16441652.[Crossref]
  3. WHO, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
  4. Halstead SB, , 1982. Immune enhancement of viral infection. Prog Allergy 31: 301364.
  5. Halstead SB, , 1989. Antibody, macrophages, dengue virus infection, shock, and hemorrhage: a pathogenetic cascade. Rev Infect Dis 11 (Suppl 4): S830S839.[Crossref]
  6. Rothman AL, , 2010. Cellular immunology of sequential dengue virus infection and its role in disease pathogenesis. Curr Top Microbiol Immunol 338: 8398.
  7. Cantelar de Francisco N, Fernandez A, Albert Molina L, Perez Balbis E, , 1981. Survey of dengue in Cuba, 1978–1979 [in Spanish]. Rev Cubana Med Trop 33: 7278.
  8. Guzman MG, Kouri GP, Bravo J, Calunga M, Soler M, Vazquez S, Venereo C, , 1984. Dengue haemorrhagic fever in Cuba. I. Serological confirmation of clinical diagnosis. Trans R Soc Trop Med Hyg 78: 235238.[Crossref]
  9. Guzman MG, Kouri G, Morier L, Soler M, Fernandez A, , 1984. A study of fatal hemorrhagic dengue cases in Cuba, 1981. Bull Pan Am Health Organ 18: 213220.
  10. Guzman MG, Kouri G, Valdes L, Bravo J, Alvarez M, Vazques S, Delgado I, Halstead SB, , 2000. Epidemiological studies on dengue in Santiago de Cuba, 1997. Am J Epidemiol 152: 793799.[Crossref]
  11. Gonzalez D, Castro OE, Kouri G, Perez J, Martinez E, Vazquez S, Rosario D, Cancio R, Guzman MG, , 2005. Classical dengue hemorrhagic fever resulting from two dengue infections spaced 20 or more years apart: Havana, dengue 3 epidemic, 2001–2002. Int J Infect Dis 9: 280285.[Crossref]
  12. Vazquez S, Bravo JR, Perez AB, Guzman MG, , 1997. Inhibition ELISA: its utility for classifying a case of dengue [in Spanish]. Rev Cubana Med Trop 49: 108112.
  13. Alvarez Vera M, Valdes Palacios D, Vazquez Ramudo S, Delgado Hernandez I, Garcia Infante S, Morier Diaz L, Guzman Tirado MG, , 1998. The standardization of the plaque reduction technique for differentiating a dengue infection from a yellow fever infection [in Spanish]. Rev Cubana Med Trop 50: 177181.
  14. Alvarez M, Rodriguez-Roche R, Bernardo L, Morier L, Guzman G, , 2005. Improved dengue virus plaque formation on BHK21 and LLCMK2 cells: evaluation of some factors. Dengue Bull 29: 4957.
  15. Morens DM, Halstead SB, Repik PM, Putvatana R, Raybourne N, , 1985. Simplified plaque reduction neutralization assay for dengue viruses by semimicro methods in BHK-21 cells: comparison of the BHK suspension test with standard plaque reduction neutralization. J Clin Microbiol 22: 250254.
  16. Alvarez Vera M, Valdes Palacios D, Vazquez Ramudo S, Delgado Hernandez I, Garcia Infante S, Morier Diaz L, Guzman Tirado MG, , 1998. The standardization of the plaque reduction technic for differentiating a dengue infection from a yellow fever infection. Rev Cubana Med Trop 50: 177181.
  17. Guzman MG, Kouri G, Bravo J, Soler M, Martinez E, , 1991. Sequential infection as risk factor for dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS) during the 1981 dengue hemorrhagic Cuban epidemic. Mem Inst Oswaldo Cruz 86: 367.[Crossref]
  18. Leclerc C, Deriaud E, Megret F, Briand JP, Van Regenmortel MH, Deubel V, , 1993. Identification of helper T cell epitopes of dengue virus E-protein. Mol Immunol 30: 613625.[Crossref]
  19. Böyusn A, , 1968. Isolation of mononuclear cells and granulocytes from human blood. Scand J Clin Lab Invest 21 (Suppl 9): 7789.
  20. Bravo JR, Guzman MG, Kouri GP, , 1987. Why dengue haemorrhagic fever in Cuba? 1. Individual risk factors for dengue haemorrhagic fever/dengue shock syndrome (DHF/DSS). Trans R Soc Trop Med Hyg 81: 816820.[Crossref]
  21. Alvarez M, Rodriguez-Roche R, Bernardo L, Vazquez S, Morier L, Gonzalez D, Castro O, Kouri G, Halstead SB, Guzman MG, , 2006. Dengue hemorrhagic fever caused by sequential dengue 1-3 virus infections over a long time interval: Havana epidemic, 2001–2002. Am J Trop Med Hyg 75: 11131117.
  22. Gibbons RV, Kalanarooj S, Jarman RG, Nisalak A, Vaughn DW, Endy TP, Mammen MP, Jr Srikiatkhachorn A, , 2007. 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 77: 910913.
  23. Guzman MG, Alvarez A, Vazquez S, Alvarez M, Rosario D, Pelaez O, Cruz G, Rodriguez-Roche R, Pavon A, Gonzalez A, Morier L, Ruiz D, Kourí G, Halstead SB, , 2012. Epidemiologic studies on dengue 3 In Playa Municipality, Havana, Cuba, 2001–2002. Int J Infect Dis 16: e198e203.[Crossref]
  24. Sierra B, Perez AB, Vogt K, Garcia G, Schmolke K, Aguirre E, Alvarez M, Kern F, Kourí G, Volk HD, Guzman MG, , 2010. Secondary heterologous dengue infection risk: disequilibrium between immune regulation and inflammation? Cell Immunol 262: 134140.[Crossref]
  25. Guzman MG, , 2005. Global voices of science. Deciphering dengue: the Cuban experience. Science 309: 14951497.[Crossref]
  26. Guzman MG, Kouri G, Bravo J, Soler M, Morier L, Vazquez S, Diaz A, Fernandez R, Ruiz A, Ramos A, , 1988. Dengue in Cuba: history of an epidemic [in Spanish]. Rev Cubana Med Trop 40: 2949.
  27. Kurane I, , 2007. Dengue hemorrhagic fever with special emphasis on immunopathogenesis. Comp Immunol Microbiol Infect Dis 30: 329340.[Crossref]
  28. Cardier JE, Marino E, Romano E, Taylor P, Liprandi F, Bosch N, Rothman AL, , 2005. Proinflammatory factors present in sera from patients with acute dengue infection induce activation and apoptosis of human microvascular endothelial cells: possible role of TNF-alpha in endothelial cell damage in dengue. Cytokine 30: 359365.[Crossref]
  29. Mangada MM, Rothman AL, , 2005. Altered cytokine responses of dengue-specific CD4+ T cells to heterologous serotypes. J Immunol 175: 26762683.[Crossref]
  30. Guidotti LG, Chisari FV, , 2001. Noncytolitic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 19: 6591.[Crossref]
  31. Gunther VJ, Putnak R, Eckels KH, Mammen MP, Schererd JM, Lyonsa A, Szteine MB, Sunf W, , 2011. A human challenge model for dengue infection reveals a possible protective role for sustained interferon gamma levels during the acute phase of illness. Vaccine 29: 38953904.[Crossref]
  32. Guzman MG, Pelaez O, Kouri G, Quintana I, Vazquez S, Penton M, Avila LC, , 2006. Final characterization of and lessons learned from the dengue 3 epidemic in Cuba, 2001–2002 [in Spanish]. Rev Panam Salud Publica 19: 282289.[Crossref]
  33. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, Suntayakorn S, Endy TP, Raengsakulrach B, Rothman AL, Ennis FA, Nisalak A, , 2000. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181: 29.[Crossref]
  34. Ocazionez RE, Gomez SY, Cortes FM, , 2007. Dengue hemorrhagic fever serotype and infection pattern in a Colombian endemic area [in Spanish]. Rev Salud Publica (Bogota) 9: 262274.[Crossref]
  35. Thomas L, Verlaeten O, Cabié A, Kaidomar S, Moravie V, Martial J, Najioullah F, Plumelle Y, Fonteau C, Dussart P, Césaire R, , 2008. Influence of the dengue serotype, previous dengue infection, and plasma viral load on clinical presentation and outcome during a dengue-2 and dengue-4 co-epidemic. Am J Trop Med Hyg 78: 990998.
  36. Tsai JJ, Chan KS, Chang JS, Chang K, Lin CC, Huang JH, Lin WR, Chen TC, Hsieh HC, Lin SH, Lin JC, Lu PL, Chen YH, Lin CY, , 2009. Effect of serotypes on clinical manifestations of dengue fever in adults. J Microbiol Immunol Infect 42: 471478.
  37. Kumaria R, , 2010. Correlation of disease spectrum among four dengue serotypes: a five years hospital based study from India. Braz J Infect Dis 14: 141146.[Crossref]
  38. Guzman MG, Deubel V, Pelegrino JL, Rosario D, Marrero M, Sariol C, Kouri G, , 1995. Partial nucleotide and amino acid sequences of the envelope and the envelope/nonstructural protein-1 gene junction of four dengue-2 virus strains isolated during the 1981 Cuban epidemic. Am J Trop Med Hyg 52: 241246.
  39. Sariol CA, Pelegrino JL, Martinez A, Arteaga E, Kouri G, Guzman MG, , 1999. Detection and genetic relationship of dengue virus sequences in seventeen-year-old paraffin-embedded samples from Cuba. Am J Trop Med Hyg 61: 9941000.
  40. Rico-Hesse R, Harrison LM, Salas RA, Tovar D, Nisalak A, Ramos C, Boshell J, de Mesa MT, Nogueira RM, da Rosa AT, , 1997. Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 230: 244251.[Crossref]
  41. Watts DM, Porter KR, Putvatana P, Vasquez B, Calampa C, Hayes CG, Halstead SB, , 1999. Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever. Lancet 354: 14311434.[Crossref]
  42. Thein S, Aung MM, Shwe TN, Aye M, Zaw A, Aye K, Aye KM, Aaskov J, , 1997. Risk factors in dengue shock syndrome. Am J Trop Med Hyg 56: 566572.
  43. Burke DS, Nisalak A, Johnson DE, Scott RM, , 1988. A prospective study of dengue infections in Bangkok. Am J Trop Med Hyg 38: 172180.
  44. Halstead SB, Schlesinger RW, , 1980. Immunological parameters of togavirus disease syndromes. , ed. The Togaviruses: Biology, Structure, Replication. New York: Academic Press, 107173.
  45. Russell PK, Yuill TM, Nisalak A, Udomsakdi S, Gould DJ, Winter PE, , 1968. An insular outbreak of dengue hemorrhagic fever. II. Virologic and serologic studies. Am J Trop Med Hyg 17: 600608.
  46. Fried JR, Gibbons RV, Kalayanarooj S, Thomas SJ, Srikiatkhachorn A, Yoon IK, Jarman RG, Green S, Rothman AL, Cummings DAT, , 2010. Serotype-specific differences in the risk of dengue hemorrhagic fever: an analysis of data collected in Bangkok, Thailand from 1994 to 2006. PLoS Negl Trop Dis 4: e617.[Crossref]
  47. Chen RF, Yang KD, Wang L, Liu JW, Chiu CC, Cheng JT, , 2007. Different clinical and laboratory manifestations between dengue haemorrhagic fever and dengue fever with bleeding tendency. Trans R Soc Trop Med Hyg 101: 11061113.[Crossref]
  48. White NJ, , 1999. Variation in virulence of dengue virus. Lancet 354: 14011402.[Crossref]
  49. Leitmeyer KC, Vaughn DW, Watts DM, Salas R, Villalobos I, de Chacon Ramos C, Rico-Hesse R, , 1999. Dengue virus structural differences that correlate with pathogenesis. J Virol 73: 47384747.
  50. Armstrong PM, Rico-Hesse R, , 2001. Differential susceptibility of Aedes aegypti to infection by the American and Southeast Asian genotypes of dengue type 2 virus. Vector Borne Zoonotic Dis 1: 159168.[Crossref]
  51. Pandey BD, Morita K, Hasebe F, Parquet MC, Igarashi A, , 2000. Molecular evolution, distribution and genetic relationship among the dengue 2 viruses isolated from different clinical severity. Southeast Asian J Trop Med Public Health 31: 266272.
  52. Pryor MJ, Carr JM, Hocking H, Davidson AD, Li P, Wright PJ, , 2001. Replication of dengue virus type 2 in human monocyte-derived macrophages: comparisons of isolates and recombinant viruses with substitutions at amino acid 390 in the envelope glycoprotein. Am J Trop Med Hyg 65: 427434.
  53. Cologna R, Rico-Hesse R, , 2003. American genotype structures decrease dengue virus output from human monocytes and dendritic cells. J Virol 77: 39293938.[Crossref]
  54. Hober D, Delannoy AS, Benyoucef S, De Groote D, Wattre P, , 1996. High levels of sTNFR p75 and TNF alpha in dengue-infected patients. Microbiol Immunol 40: 569573.[Crossref]
  55. Hober D, Nguyen TL, Shen L, Ha DQ, Huong VT, Benyoucef S, Nguyen TH, Bui TM, Loan HK, Le BL, Bouzidi A, De Groote D, Drouet MT, Deubel V, Wattre P, , 1998. Tumor necrosis factor alpha levels in plasma and whole-blood culture in dengue-infected patients: relationship between virus detection and pre-existing specific antibodies. J Med Virol 54: 210218.[Crossref]
  56. Hober D, Poli L, Roblin B, Gestas P, Chungue E, Granic G, Imbert P, Pecarere JL, Vergez-Pascal R, Wattre P, , 1993. Serum levels of tumor necrosis factor-alpha (TNF-alpha), interleukin-6 (IL-6), and interleukin-1 beta (IL-1 beta) in dengue-infected patients. Am J Trop Med Hyg 48: 324331.
  57. Suharti C, Van Gorp EC, Setiati TE, Dolmans WM, Djokomoeljanto RJ, Hack CE, Ten CH, Van der Meer JW, , 2002. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost 87: 4246.
  58. Gagnon SJ, Mori M, Kurane I, Green S, Vaughn DW, Kalayanarooj S, Suntayakorn S, Ennis FA, Rothman AL, , 2002. Cytokine gene expression and protein production in peripheral blood mononuclear cells of children with acute dengue virus infections. J Med Virol 67: 4146.[Crossref]
  59. Rothman AL, , 2009. T lymphocyte responses to heterologous secondary dengue virus infections. Ann N Y Acad Sci 1171: E36E41.[Crossref]
  60. Mathew A, Rothman AL, , 2008. Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunological Rew 225: 300313.[Crossref]
  61. Dong T, Moran E, Vinh Chau N, Simmons C, Luhn K, Peng Y, Wills B, Phuong Dung N, Thi Thu Thao L, Hien TT, McMichael A, Farrar J, Rowland-Jones S, , 2007. High pro-inflammatory cytokine secretion and loss of high avidity cross-reactive cytotoxic T-cells during the course of secondary dengue virus infection. PLoS ONE 2: e1192.[Crossref]
  62. Rothman AL, , 2003. Immunology and immunopathogenesis of dengue disease. Adv Virus Res 60: 397419.[Crossref]
  63. Kurane I, Innis BL, Nimmannitya S, Nisalak A, Rothman AL, Livingston PG, Janus J, Ennis FA, , 1990. Human immune responses to dengue viruses. Southeast Asian J Trop Med Public Health 21: 658662.
  64. Kurane I, Innis BL, Nimmannitya S, Nisalak A, Meager A, Janus J, Ennis FA, , 1991. Activation of T lymphocytes in dengue virus infections. High levels of soluble interleukin 2 receptor, soluble CD4, soluble CD8, interleukin 2, and interferon-gamma in sera of children with dengue. J Clin Invest 88: 14731480.[Crossref]
  65. Green S, Pichyangkul S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Nisalak A, Kurane I, Rothman AL, Ennis FA, , 1999. Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis 180: 14291435.[Crossref]
  66. Green S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Suntayakorn S, Nisalak A, Lew R, Innis BL, Kurane I, Rothman AL, Ennis FA, , 1999. Early immune activation in acute dengue illness is related to development of plasma leakage and disease severity. J Infect Dis 179: 755762.[Crossref]
  67. Guzman MG, Kouri G, Valdes L, Bravo J, Vazquez S, Halstead SB, , 2002. Enhanced severity of secondary dengue-2 infections: death rates in 1981 and 1997 Cuban outbreaks. Rev Panam Salud Publica 11: 223227.[Crossref]
  68. Guzman MG, Kouri G, Bravo J, Valdes L, Vazquez S, Halstead SB, , 2002. Effect of age on outcome of secondary dengue 2 infections. Int J Infect Dis 6: 118124.[Crossref]
  69. Halstead SB, , 2002. Dengue. Curr Opin Infect Dis 15: 471476.
  70. Guzman MG, Kouri GP, Bravo J, Soler M, Vazquez S, Santos M, Villaescusa R, Basanta P, Indan G, Ballester JM, , 1984. Dengue haemorrhagic fever in Cuba. II. Clinical investigations. Trans R Soc Trop Med Hyg 78: 239241.[Crossref]
  71. Kouri G, Guzman MG, Bravo J, , 1986. Hemorrhagic dengue in Cuba: history of an epidemic. Bull Pan Am Health Organ 20: 2430.
  72. Jinquan T, Larsen CG, Gesser B, Matsushima K, Thestrup-Pedersen K, , 1993. Human IL-10 is a chemoattractant for CD8+ T lymphocytes and an inhibitor of IL-8-induced CD4+ T lymphocyte migration. J Immunol 151: 45454551.
  73. Vora M, Romero LI, Karasek MA, , 1996. Interleukin-10 induces E-selectin on small and large blood vessel endothelial cells. J Exp Med 184: 821829.[Crossref]
  74. Santin AD, Hermonat PL, Ravaggi A, Bellone S, Pecorelli S, Roman JJ, Parham GP, Cannon MJ, , 2000. Interleukin-10 increases Th1 cytokine production and cytotoxic potential in human papillomavirus-specific CD8(+) cytotoxic T lymphocytes. J Virol 74: 47294737.[Crossref]
  75. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA, , 2006. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24: 99146.[Crossref]
  76. Taylor AW, , 2009. Review of the activation of TGF-beta in immunity. J Leukoc Biol, 2009 Jan; 85 (1): 2933.
  77. Gil L, López C, Lazo L, Valdés I, Marcos E, Alonso R, Gambe A, Martin J, Romero Y, Guzmán M, Guillén G, Hermida L, , 2009. Recombinant nucleocapsid-like particles from dengue-2 virus induce protective CD4+ and CD8+ cells against viral encephalitis in mice. Int Immunol 21: 11751183.[Crossref]
  78. Yauch LE, Zellweger RM, Kotturi MF, Qutubuddin A, Sidney J, Peters B, Prestwood TR, Sette A, Shresta S, , 2009. A protective role for dengue virus-specific CD8+ T cells. J Immunol 182: 48654873.[Crossref]
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  • Received : 16 Aug 2011
  • Accepted : 04 May 2012

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