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DOI: 10.1160/TH09-03-0208
Plasma leakage in dengue haemorrhagic fever
Financial support: This work was supported by National Institutes of Health Grant NIH-P01AI34533.Publication History
Received:
31 March 2009
Accepted after major revision:
06 September 2009
Publication Date:
28 November 2017 (online)
Summary
Dengue viruses (DENV), a group of four serologically distinct but related flaviviruses, are the cause of one of the most important emerging viral diseases. DENV infections result in a wide spectrum of clinical disease including dengue haemorrhagic fever (DHF), a viral haemorrhagic disease characterised by bleeding and plasma leakage.The characteristic feature of DHF is the transient period of plasma leakage and a haemorrhagic tendency. DHF occurs mostly during a secondary DENV infection. Serotype cross-reactive antibodies and mediators from serotype cross-reactive Dengue-specific T cells have been impli-cated in the pathogenesis. A complex interaction between virus, host immune response and endothelial cells likely impacts the barrier integrity and functions of endothelial cells leading to plasma leakage. Recently the role of angiogenic factors and the role of dengue virus on endothelial cell transcription and functions have been studied. Insights into the mechanisms that confer protection or cause disease are critical in the development of prophylactic and therapeutic modalities for this important disease.
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References
- 1 Organization WH. Dengue and dengue haemorrhagic fever. ( http://wwwwhoint/mediacentre/fact-sheets/fs117/en/ accessed 1 December 2008)
- 2 Organization WH. editor. Dengue and dengue haemorrhagic fever. WHO; Geneva: 2000
- 3 Pinheiro FP, Corber SJ. Global situation of dengue and dengue haemorrhagic fever, and its emergence in the Americas. World Health Stat Q 1997; 50: 161-169.
- 4 Kouri G, Guzman MG, Valdes L. et al. Reemergence of dengue in Cuba: a 1997 epidemic in Santiago de Cuba. Emerg Infect Dis 1998; 04: 89-92.
- 5 Gubler D, Kuno G, Markoff L. Flavivirus Field’s Virology. 5th ed. Lippincott Williams & Wilkins; 2007
- 6 Lindenbach BD, Thiel H-J, Rice CM. Flaviviridae: The Viruses and Their Replication, Field’s Virology. Lippincott Williams & Wilkins; 2007
- 7 Jones M, Davidson A, Hibbert L. et al. Dengue virus inhibits alpha interferon signaling by reducing STAT2 expression. J Virol 2005; 79: 5414-5420.
- 8 Munoz-Jordan JL, Laurent-Rolle M, Ashour J. et al. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J Virol 2005; 79: 8004-8013.
- 9 Medin CL, Fitzgerald KA, Rothman AL. Dengue virus nonstructural protein NS5 induces interleukin-8 transcription and secretion. J Virol 2005; 79: 11053-11061.
- 10 Avirutnan P, Punyadee N, Noisakran S. et al. Vascular leakage in severe dengue virus infections: a potential role for the nonstructural viral protein NS1 and complement. The Journal of infectious diseases 2006; 193: 1078-1088.
- 11 Organization WH. Dengue Hemorrhagic Fever: diagnosis, treatment, prevention and control. 2nd ed. WHO, WHO; 1997.;
- 12 Pancharoen C, Rungsarannont A, Thisyakorn U. Hepatic dysfunction in dengue patients with various severity. J Med Assoc Thai 2002; 85 (Suppl. 01) S298-301.
- 13 Cam BV, Fonsmark L, Hue NB. et al. Prospective case-control study of encephalopathy in children with dengue hemorrhagic fever. Am J Tropical Med Hyg 2001; 65: 848-851.
- 14 Janssen HL, Bienfait HP, Jansen CL. et al. Fatal cerebral oedema associated with primary dengue infection. J Infect 1998; 36: 344-346.
- 15 Srikiatkhachorn A, Krautrachue A, Ratanaprakarn W. et al. Natural history of plasma leakage in dengue hemorrhagic fever: a serial ultrasonographic study. The Pediatric infectious disease journal 2007; 26: 283-292.
- 16 Balasubramanian S, Janakiraman L, Kumar SS. et al. A reappraisal of the criteria to diagnose plasma leakage in dengue hemorrhagic fever. Indian Ped 2006; 43: 334-339.
- 17 Krishnamurti C, Kalayanarooj S, Cutting MA. et al. Mechanisms of hemorrhage in dengue without circulatory collapse. Am J Tropical Med Hyg 2001; 65: 840-847.
- 18 Nimmannitya S. Clinical manifestations of Dengue/Dengue Haemorrhagic Fever. In: Monograph on Dengue/Dengue Haemorrhagic Fever. World Health Organization; New Delhi: 1993: 48-57.
- 19 Wills BA, Nguyen MD, Ha TL. et al. Comparison of three fluid solutions for resuscitation in dengue shock syndrome. New Engl J Med 2005; 353: 877-889.
- 20 Burke DS, Nisalak A, Johnson DE. et al. A prospective study of dengue infections in Bangkok. Am J Tropical Med Hyg 1988; 38: 172-180.
- 21 Endy TP, Chunsuttiwat S, Nisalak A. 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: 40-51.
- 22 Halstead SB, O’Rourke EJ. Antibody-enhanced dengue virus infection in primate leukocytes. Nature 1977; 265: 739-741.
- 23 Halstead SB. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 1979; 140: 527-533.
- 24 Stephens HA, Klaythong R, Sirikong M. et al. HLA-A and -B allele associations with secondary dengue virus infections correlate with disease severity and the infecting viral serotype in ethnic Thais. Tissue Antigens 2002; 60: 309-318.
- 25 Soundravally R, Hoti SL. Polymorphisms of the TAP 1 and 2 gene may influence clinical outcome of primary dengue viral infection. Scand J Immunol 2008; 67: 618-625.
- 26 Sakuntabhai A, Turbpaiboon C, Casademont I. et al. A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet 2005; 37: 507-513.
- 27 Fernandez-Mestre MT, Gendzekhadze K, RivasVetencourt P. et al. TNF-alpha-308A allele, a possible severity risk factor of hemorrhagic manifestation in dengue fever patients. Tissue Antigens 2004; 64: 469-472.
- 28 Rico-Hesse R, Harrison LM, Salas RA. et al. Origins of dengue type 2 viruses associated with increased pathogenicity in the Americas. Virology 1997; 230: 244-251.
- 29 Kochel TJ, Watts DM, Halstead SB. et al. Effect of dengue-1 antibodies on American dengue-2 viral infection and dengue haemorrhagic fever. Lancet 2002; 360: 310-312.
- 30 Rodrigo WW, Alcena DC, Kou Z. et al. Difference between the abilities of human Fcgamma receptor-expressing CV-1 cells to neutralize American and Asian genotypes of dengue virus 2. Clin Vaccine Immunol 2009; 16: 285-287.
- 31 Holden KL, Harris E. Enhancement of dengue virus translation: role of the 3’ untranslated region and the terminal 3’ stem-loop domain. Virology 2004; 329: 119-133.
- 32 Leitmeyer KC, Vaughn DW, Watts DM. et al. Dengue virus structural differences that correlate with pathogenesis. J Virology 1999; 73: 4738-4747.
- 33 Barth OM, Barreto DF, Paes MV. et al. Morphological studies in a model for dengue-2 virus infection in mice. Mem Inst Oswaldo Cruz 2006; 101: 905-915.
- 34 Kyle JL, Beatty PR, Harris E. Dengue virus infects macrophages and dendritic cells in a mouse model of infection. J Infect Dis 2007; 195: 1808-1817.
- 35 Shresta S, Sharar KL, Prigozhin DM. et al. Murine model for dengue virus-induced lethal disease with increased vascular permeability. J Virology 2006; 80: 10208-10217.
- 36 Mota J, Rico-Hesse R. Humanized mice show clinical signs of dengue fever according to infecting virus genotype. J Virology 2009; 83: 8638-8645.
- 37 Bente DA, Melkus MW, Garcia JV. et al. Dengue fever in humanized NOD/SCID mice. J Virology 2005; 79: 13797-13799.
- 38 Bhamarapravati N, Tuchinda P, Boonyapaknavik V. Pathology of Thailand haemorrhagic fever: a study of 100 autopsy cases. Ann Trop Med Parasitol 1967; 61: 500-510.
- 39 Jessie K, Fong MY, Devi S. et al. Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 2004; 189: 1411-1418.
- 40 Balsitis SJ, Coloma J, Castro G. et al. Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. The American journal of tropical medicine and hygiene 2009; 80: 416-424.
- 41 Limonta D, Capo V, Torres G. et al. Apoptosis in tissues from fatal dengue shock syndrome. J Clin Virol 2007; 40: 50-54.
- 42 Marovich M, Grouard-Vogel G, Louder M. et al. Human dendritic cells as targets of dengue virus infection. J Investig Dermatol Symp Proc 2001; 06: 219-224.
- 43 Tassaneetrithep B, Burgess TH, Granelli-Piperno A. et al. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 2003; 197: 823-829.
- 44 Pokidysheva E, Zhang Y, Battisti AJ. et al. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 2006; 124: 485-493.
- 45 Libraty DH, Pichyangkul S, Ajariyakhajorn C. et al. Human dendritic cells are activated by dengue virus infection: enhancement by gamma interferon and implications for disease pathogenesis. Journal of virology 2001; 75: 3501-358.
- 46 Ho LJ, Wang JJ, Shaio MF. et al. Infection of human dendritic cells by dengue virus causes cell maturation and cytokine production. J Immunol 2001; 166: 1499-1506.
- 47 Taweechaisupapong S, Sriurairatana S, Angsubhakorn S. et al. In vivo and in vitro studies on the morphological change in the monkey epidermal Langerhans cells following exposure to dengue 2 (16681) virus. Southeast Asian J Trop Med Public Health 1996; 27: 664-672.
- 48 Wu SJ, Grouard-Vogel G, Sun W. et al. Human skin Langerhans cells are targets of dengue virus infection. Nat Med 2000; 06: 816-820.
- 49 Libraty DH, Endy TP, Houng HS. et al. Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis 2002; 185: 1213-1221.
- 50 Vaughn DW, Green S, Kalayanarooj S. et al. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 2000; 181: 2-9.
- 51 Libraty DH, Young PR, Pickering D. et al. High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J Infect Dis 2002; 186: 1165-1168.
- 52 Bosch I, Xhaja K, Estevez L. et al. Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J Virology 2002; 76: 5588-5597.
- 53 Carr JM, Hocking H, Bunting K. et al. Supernatants from dengue virus type-2 infected macrophages induce permeability changes in endothelial cell monolayers. J Med Virol 2003; 69: 521-528.
- 54 Lee YR, Liu MT, Lei HY. et al. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/ dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 2006; 87: 3623-3630.
- 55 Cardier JE, Marino E, Romano E. et al. 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 2005; 30: 359-365.
- 56 Avirutnan P, Malasit P, Seliger B. et al. Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 1998; 161: 6338-6346.
- 57 Green S, Pichyangkul S, Vaughn DW. et al. Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis 1999; 180: 1429-1435.
- 58 Mathew A, Kurane I, Green S. et al. Predominance of HLA-restricted cytotoxic T-lymphocyte responses to serotype-cross-reactive epitopes on nonstructural proteins following natural secondary dengue virus infection. J Virology 1998; 72: 3999-4004.
- 59 Mongkolsapaya J, Dejnirattisai W, Xu XN. et al. Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 2003; 09: 921-927.
- 60 Mongkolsapaya J, Duangchinda T, Dejnirattisai W. et al. T cell responses in dengue hemorrhagic fever: are cross-reactive T cells suboptimal?. J Immunol 2006; 176: 3821-3829.
- 61 Dong T, Moran E, Vinh NChau. et al. 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 2007; 02: e1192.
- 62 Beaumier CM, Mathew A, Bashyam HS. et al. Cross-reactive memory CD8(+) T cells alter the immune response to heterologous secondary dengue virus infections in mice in a sequence-specific manner. J Infect Dis 2008; 197: 608-617.
- 63 Bashyam HS, Green S, Rothman AL. Dengue virus-reactive CD8+ T cells display quantitative and qualitative differences in their response to variant epitopes of heterologous viral serotypes. J Immunol 2006; 176: 2817-2824.
- 64 Mangada MM, Rothman AL. Altered cytokine responses of dengue-specific CD4+ T cells to heterologous serotypes. J Immunol 2005; 175: 2676-2683.
- 65 Lin CF, Lei HY, Shiau AL. et al. Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J Med Virol 2003; 69: 82-90.
- 66 Lin CF, Lei HY, Shiau AL. et al. Endothelial cell apoptosis induced by antibodies against dengue virus nonstructural protein 1 via production of nitric oxide. J Immunol 2002; 169: 657-664.
- 67 Lin CF, Wan SW, Chen MC. et al. Liver injury caused by antibodies against dengue virus nonstructural protein 1 in a murine model. Lab Invest 2008; 88: 1079-1089.
- 68 Falconar AK. The dengue virus nonstructural-1 protein (NS1) generates antibodies to common epitopes on human blood clotting, integrin/adhesin proteins and binds to human endothelial cells: potential implications in haemorrhagic fever pathogenesis. Arch Virol 1997; 142: 897-916.
- 69 Sun DS, King CC, Huang HS. et al. Antiplatelet autoantibodies elicited by dengue virus non-structural protein 1 cause thrombocytopenia and mortality in mice. J Thromb Haemost 2007; 05: 2291-2299.
- 70 Yen YT, Chen HC, Lin YD. et al. Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virology 2008; 82: 12312-12324.
- 71 Chen HC, Hofman FM, Kung JT. et al. Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virology 2007; 81: 5518-5526.
- 72 Warke RV, Xhaja K, Martin KJ. et al. Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells. J Virology 2003; 77: 11822-11832.
- 73 Huang YH, Lei HY, Liu HS. et al. Dengue virus infects human endothelial cells and induces IL-6 and IL-8 production. Am J Tropical Med Hyg 2000; 63: 71-75.
- 74 Jiang Z, Tang X, Xiao R. et al. Dengue virus regulates the expression of hemostasis-related molecules in human vein endothelial cells. J Infect 2007; 55: e23-28.
- 75 Huang YH, Lei HY, Liu HS. et al. Tissue plasminogen activator induced by dengue virus infection of human endothelial cells. J Med Virol 2003; 70: 610-616.
- 76 Huerta-Zepeda A, Cabello-Gutierrez C, Cime-Castillo J. et al. Crosstalk between coagulation and inflammation during Dengue virus infection. Thromb Haemost 2008; 99: 936-943.
- 77 Cabello-Gutierrez C, Manjarrez-Zavala ME, Huerta-Zepeda A. et al. Modification of the cytoprotective protein C pathway during Dengue virus infection of human endothelial vascular cells. Thromb Haemost 2009; 101: 916-928.
- 78 Butthep P, Chunhakan S, Tangnararatchakit K. et al. Elevated soluble thrombomodulin in the febrile stage related to patients at risk for dengue shock syndrome. Ped Infect Dis J 2006; 25: 894-897.
- 79 Anderson R, Wang S, Osiowy C. et al. Activation of endothelial cells via antibody-enhanced dengue virus infection of peripheral blood monocytes. J Virology 1997; 71: 4226-4232.
- 80 Peyrefitte CN, Pastorino B, Grau GE. et al. Dengue virus infection of human microvascular endothelial cells from different vascular beds promotes both common and specific functional changes. J Med Virol 2006; 78: 229-242.
- 81 Zhang JL, Wang JL, Gao N. et al. Up-regulated expression of beta3 integrin induced by dengue virus serotype 2 infection associated with virus entry into human dermal microvascular endothelial cells. Biochem Biophys Res Commun 2007; 356: 763-768.
- 82 Srikiatkhachorn A, Ajariyakhajorn C, Endy TP. et al. Virus-induced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic Fever. J Virology 2007; 81: 1592-1600.
- 83 Luplertlop N, Misse D, Bray D. et al. Dengue-virusinfected dendritic cells trigger vascular leakage through metalloproteinase overproduction. EMBO Rep 2006; 07: 1176-1181.
- 84 Luplertlop N, Misse D. MMP cellular responses to dengue virus infection-induced vascular leakage. Jpn J Infect Dis 2008; 61: 298-301.
- 85 Dewi BE, Takasaki T, Kurane I. Peripheral blood mononuclear cells increase the permeability of dengue virus-infected endothelial cells in association with downregulation of vascular endothelial cadherin. J Gen Virol 2008; 89: 642-652.
- 86 Schnittler HJ, Feldmann H. Viral hemorrhagic fever-a vascular disease?. Thromb Haemost 2003; 89: 967-972.
- 87 Zampieri CA, Sullivan NJ, Nabel GJ. Immunopathology of highly virulent pathogens: insights from Ebola virus. Nature Immunol 2007; 08: 1159-1164.
- 88 Zaki SR, Greer PW, Coffield LM. et al. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol 1995; 146: 552-579.
- 89 Agarwal R, Elbishbishi EA, Chaturvedi UC. et al. Profile of transforming growth factor-beta 1 in patients with dengue haemorrhagic fever. Int J Exp Pathol 1999; 80: 143-149.
- 90 Laur F, Murgue B, Deparis X. et al. Plasma levels of tumour necrosis factor alpha and transforming growth factor beta-1 in children with dengue 2 virus infection in French Polynesia. Transact Royal Soc Trop Med Hyg 1998; 92: 654-656.
- 91 Sironen T, Klingstrom J, Vaheri A. et al. Pathology of Puumala hantavirus infection in macaques. PloS one 2008; 03: e3035.
- 92 Kilpatrick ED, Terajima M, Koster FT. et al. Role of specific CD8+ T cells in the severity of a fulminant zoonotic viral hemorrhagic fever, hantavirus pulmonary syndrome. J Immunol 2004; 172: 3297-3304.