ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Braga EL, Moura P, Pinto LM, Ignacio SR, Oliveira MJ, Cordeiro MT, Kubelka CF, 2001. Detection of circulant tumor necrosis factor-alpha, soluble tumor necrosis factor p75 and interferon-gamma in Brazilian patients with dengue fever and dengue hemorrhagic fever. Mem Inst Oswaldo Cruz 96: 229–232.
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Brasier AR, Garcia J, Wiktorowicz JE, Spratt HM, Comach G, Ju H, Recinos A 3rd, Soman K, Forshey BM, Halsey ES, Blair PJ, Rocha C, Bazan I, Victor SS, Wu Z, Stafford S, Watts D, Morrison AC, Scott TW, Kochel TJ; Venezuelan Dengue Fever Working G, 2012. Discovery proteomics and nonparametric modeling pipeline in the development of a candidate biomarker panel for dengue hemorrhagic fever. Clin Transl Sci 5: 8–20.
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Braiser AR, Ju H, Garcia J, Spratt HM, Victor SS, Forshey BM, Halsey ES, Comach G, Sierra G, Blair PJ, Rocha C, Morrison AC, Scott TW, Bazan I, Kochel TJ, Venezuelan Dengue Fever Working Group, 2012. A three-component biomarker panel for prediction of dengue hemorrhagic fever. Am J Trop Med Hyg 86: 341–348.
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Koraka P, Lim YP, Shin MD, Setiati TE, Mairuhu AT, van Gorp EC, Soemantri A, Osterhaus AD, Martina BE, 2010. Plasma levels of inter-alpha inhibitor proteins in children with acute dengue virus infection. PLoS ONE 5: e9967.
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Calzavara-Silva CE, Gomes AL, Maia RC, Acioli-Santos B, Gil LH, Marques ET Jr, 2009. Early molecular markers predictive of dengue hemorrhagic fever. An Acad Bras Cienc 81: 671–677.
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Silva MM, Gil LH, Marques ET Jr, Calzavara-Silva CE, 2013. Potential biomarkers for the clinical prognosis of severe dengue. Mem Inst Oswaldo Cruz 108: 755–762.
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Sun P, Garcia J, Comach G, Vahey MT, Wang Z, Forshey BM, Morrison AC, Sierra G, Bazan I, Rocha C, Vilcarromero S, Blair PJ, Scott TW, Camacho DE, Ockenhouse CF, Halsey ES, Kochel TJ, 2013. Sequential waves of gene expression in patients with clinically defined dengue illnesses reveal subtle disease phases and predict disease severity. PLoS Negl Trop Dis 7: e2298.
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Malavige GN, Gomes L, Alles L, Chang T, Salimi M, Fernando S, Nanayakkara KD, Jayaratne S, Ogg GS, 2013. Serum IL-10 as a marker of severe dengue infection. BMC Infect Dis 13: 341.
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Rathakrishnan A, Wang SM, Hu Y, Khan AM, Ponnampalavanar S, Lum LC, Manikam R, Sekaran SD, 2012. Cytokine expression profile of dengue patients at different phases of illness. PLoS ONE 7: e52215.
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Kumar Y, Liang C, Bo Z, Rajapakse JC, Ooi EE, Tannenbaum SR, 2012. Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLoS Negl Trop Dis 6: e1887.
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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: 2–9.
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Sudiro TM, Zivny J, Ishiko H, Green S, Vaughn DW, Kalayanarooj S, Nisalak A, Norman JE, Ennis FA, Rothman AL, 2001. Analysis of plasma viral RNA levels during acute dengue virus infection using quantitative competitor reverse transcription-polymerase chain reaction. J Med Virol 63: 29–34.
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Hodgetts A, Levin M, Kroll JS, Langford PR, 2007. Biomarker discovery in infectious diseases using SELDI. Future Microbiol 2: 35–49.
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Johnson BW, Russell BJ, Lanciotti RS, 2005. Serotype-specific detection of dengue viruses in a fourplex real-time reverse transcriptase PCR assay. J Clin Microbiol 43: 4977–4983.
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Martin JN, Amad Z, Cossen C, Lam PK, Kedes DH, Page-Shafer KA, Osmond DH, Forghani B, 2000. Use of epidemiologically well-defined subjects and existing immunofluorescence assays to calibrate a new enzyme immunoassay for human herpes virus 8 antibodies. J Clin Microbiol 38: 696–701.
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Martin DA, Muth DA, Brown T, Johnson AJ, Karabatsos N, Roehrig JT, 2000. Standardization of immunoglobulin M capture enzyme-linked immunosorbent assays for routine diagnosis of arboviral infections. J Clin Microbiol 38: 1823–1826.
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Ndao M, Spithill TW, Caffrey R, Li H, Podust VN, Perichon R, Santamaria C, Ache A, Duncan M, Powell MR, Ward BJ, 2010. Identification of novel diagnostic serum biomarkers for Chagas' disease in asymptomatic subjects by mass spectrometric profiling. J Clin Microbiol 48: 1139–1149.
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Discovery and Characterization of Potential Prognostic Biomarkers for Dengue Hemorrhagic Fever
B. Katherine Poole-Smith
B. Katherine Poole-Smith
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Alexa Gilbert
Alexa Gilbert
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Andrea L. Gonzalez
Andrea L. Gonzalez
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Manuela Beltran
Manuela Beltran
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Kay M. Tomashek
Kay M. Tomashek
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Brian J. Ward
Brian J. Ward
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Elizabeth A. Hunsperger
Elizabeth A. Hunsperger
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Momar Ndao
Momar Ndao
Division of Vector-Borne Diseases, Dengue Branch, Centers for Disease Control and Prevention, San Juan, Puerto Rico; National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal General Hospital R3-137, Montreal, Quebec H3G 1A4, Canada; 3FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec H3G 1A4, Canada
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Half a million patients are hospitalized with severe dengue every year, many of whom would die without timely, appropriate clinical intervention. The majority of dengue cases are uncomplicated; however, 2–5% progress to severe dengue. Severe dengue cases have been reported with increasing frequency over the last 30 years. To discover biomarkers for severe dengue, we used surface-enhanced laser desorption/ionization time-of-flight mass spectrometry to analyze dengue virus positive serum samples from the acute phase of infection. Using this method, 16 proteins were identified as candidate biomarkers for severe dengue. From these 16 biomarkers, three candidates were selected for confirmation by enzyme-linked immunosorbent assay and Western blot: vitronectin (Vtn, 55.1 kDa), hemopexin (Hx, 52.4 kDa), and serotransferrin (Tf, 79.2 kDa). Vitronectin, Hx, and Tf best differentiated between dengue and severe dengue.
Author Notes
Financial support: This work was supported by the Centers for Disease Control and Prevention, the Sandler Foundation, the Foundation of the Montreal General Hospital and the Research Institute of the McGill University Health Centre.
Disclosure: B. Katherine Poole-Smith, Kay M. Tomashek, Elizabeth A. Hunsperger, and Momar Ndao are inventors on a patent “Detection of subject biomarker diagnostic assay for dengue fever and the differentiation of dengue hemorrhagic fever.” United States Patent WO/2013/130029 Sept 6, 2013. Momar Ndao and Brian J. Ward are inventors on a patent entitled “Biomarkers for Dengue. United States Patent US 2012/0021936 A1 Jan 26, 2012. B. Katherine Poole-Smith, Manuela Beltran, Kay M. Tomashek, and Elizabeth A. Hunsperger are employees of the U.S. Government. This work was prepared as part of their official duties.
Authors' addresses: B. Katherine Poole-Smith, Manuela Beltran, Kay M. Tomashek, and Elizabeth A. Hunsperger, Dengue Branch, Centers for Disease Control and Prevention, San Juan, PR, E-mails: isd5@cdc.gov, mvb6@cdc.gov, kct9@cdc.gov, and enh4@cdc.gov. Alexa Gilbert, AssureRx Canada, Toronto, Ontario, Canada, E-mail: alexa.gilbert@mail.mcgill.ca. Andrea L. Gonzalez, Environmental Health, University of Puerto Rico Graduate School of Public Health, San Juan, PR, E-mail: andrea.l.gonzalez@upr.edu. Brian J. Ward, National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada, E-mail: brian.ward@mcgill.ca. Momar Ndao, National Reference Centre for Parasitology, Research Institute of the McGill University Health Centre, Montreal, Quebec, Canada, and FQRNT Centre for Host–Parasite Interactions, McGill University, Montreal, Quebec, Canada, E-mail: momar.ndao@mcgill.ca.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
WHO, 1997. Dengue Hemorrhagic Fever: Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization.
-
2.
Peeling RW, Artsob H, Pelegrino JL, Buchy P, Cardosa MJ, Devi S, Enria DA, Farrar J, Gubler DJ, Guzman MG, Halstead SB, Hunsperger E, Kliks S, Margolis HS, Nathanson CM, Nguyen VC, Rizzo N, Vazquez S, Yoksan S, 2010. Evaluation of diagnostic tests: dengue. Nat Rev Microbiol 8: S30–S38.
-
3.
WHO, 2009. Clinical management and delivery of clinical services. Ciceri K & Tissot P Dengue Guidelines for Diagnosis, Treatment, Prevention and Control. Geneva: World Health Organization, 23–55.
-
4.
Levy A, Valero N, Espina LM, Anez G, Arias J, Mosquera J, 2010. Increment of interleukin 6, tumor necrosis factor alpha, nitric oxide, C-reactive protein and apoptosis in dengue. Trans R Soc Trop Med Hyg 104: 16–23.
-
5.
Braga EL, Moura P, Pinto LM, Ignacio SR, Oliveira MJ, Cordeiro MT, Kubelka CF, 2001. Detection of circulant tumor necrosis factor-alpha, soluble tumor necrosis factor p75 and interferon-gamma in Brazilian patients with dengue fever and dengue hemorrhagic fever. Mem Inst Oswaldo Cruz 96: 229–232.
-
6.
Brasier AR, Garcia J, Wiktorowicz JE, Spratt HM, Comach G, Ju H, Recinos A 3rd, Soman K, Forshey BM, Halsey ES, Blair PJ, Rocha C, Bazan I, Victor SS, Wu Z, Stafford S, Watts D, Morrison AC, Scott TW, Kochel TJ; Venezuelan Dengue Fever Working G, 2012. Discovery proteomics and nonparametric modeling pipeline in the development of a candidate biomarker panel for dengue hemorrhagic fever. Clin Transl Sci 5: 8–20.
-
7.
Braiser AR, Ju H, Garcia J, Spratt HM, Victor SS, Forshey BM, Halsey ES, Comach G, Sierra G, Blair PJ, Rocha C, Morrison AC, Scott TW, Bazan I, Kochel TJ, Venezuelan Dengue Fever Working Group, 2012. A three-component biomarker panel for prediction of dengue hemorrhagic fever. Am J Trop Med Hyg 86: 341–348.
-
8.
Koraka P, Lim YP, Shin MD, Setiati TE, Mairuhu AT, van Gorp EC, Soemantri A, Osterhaus AD, Martina BE, 2010. Plasma levels of inter-alpha inhibitor proteins in children with acute dengue virus infection. PLoS ONE 5: e9967.
-
9.
Murgue B, Cassar O, Deparis X, 2001. Plasma concentrations of sVCAM-1 and severity of dengue infections. J Med Virol 65: 97–104.
-
10.
Devignot S, Sapet C, Duong V, Bergon A, Rihet P, Ong S, Lorn PT, Chroeung N, Ngeav S, Tolou HJ, Buchy P, Couissinier-Paris P, 2010. Genome-wide expression profiling deciphers host responses altered during dengue shock syndrome and reveals the role of innate immunity in severe dengue. PLoS ONE 5: e11671.
-
11.
Calzavara-Silva CE, Gomes AL, Maia RC, Acioli-Santos B, Gil LH, Marques ET Jr, 2009. Early molecular markers predictive of dengue hemorrhagic fever. An Acad Bras Cienc 81: 671–677.
-
12.
Silva MM, Gil LH, Marques ET Jr, Calzavara-Silva CE, 2013. Potential biomarkers for the clinical prognosis of severe dengue. Mem Inst Oswaldo Cruz 108: 755–762.
-
13.
Sun P, Garcia J, Comach G, Vahey MT, Wang Z, Forshey BM, Morrison AC, Sierra G, Bazan I, Rocha C, Vilcarromero S, Blair PJ, Scott TW, Camacho DE, Ockenhouse CF, Halsey ES, Kochel TJ, 2013. Sequential waves of gene expression in patients with clinically defined dengue illnesses reveal subtle disease phases and predict disease severity. PLoS Negl Trop Dis 7: e2298.
-
14.
Malavige GN, Gomes L, Alles L, Chang T, Salimi M, Fernando S, Nanayakkara KD, Jayaratne S, Ogg GS, 2013. Serum IL-10 as a marker of severe dengue infection. BMC Infect Dis 13: 341.
-
15.
Rathakrishnan A, Wang SM, Hu Y, Khan AM, Ponnampalavanar S, Lum LC, Manikam R, Sekaran SD, 2012. Cytokine expression profile of dengue patients at different phases of illness. PLoS ONE 7: e52215.
-
16.
Pawitan JA, 2011. Dengue virus infection: predictors for severe dengue. Acta Med Indones 43: 129–135.
-
17.
Kumar Y, Liang C, Bo Z, Rajapakse JC, Ooi EE, Tannenbaum SR, 2012. Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLoS Negl Trop Dis 6: e1887.
-
18.
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: 2–9.
-
19.
Sudiro TM, Zivny J, Ishiko H, Green S, Vaughn DW, Kalayanarooj S, Nisalak A, Norman JE, Ennis FA, Rothman AL, 2001. Analysis of plasma viral RNA levels during acute dengue virus infection using quantitative competitor reverse transcription-polymerase chain reaction. J Med Virol 63: 29–34.
-
20.
Hodgetts A, Levin M, Kroll JS, Langford PR, 2007. Biomarker discovery in infectious diseases using SELDI. Future Microbiol 2: 35–49.
-
21.
Johnson BW, Russell BJ, Lanciotti RS, 2005. Serotype-specific detection of dengue viruses in a fourplex real-time reverse transcriptase PCR assay. J Clin Microbiol 43: 4977–4983.
-
22.
Martin JN, Amad Z, Cossen C, Lam PK, Kedes DH, Page-Shafer KA, Osmond DH, Forghani B, 2000. Use of epidemiologically well-defined subjects and existing immunofluorescence assays to calibrate a new enzyme immunoassay for human herpes virus 8 antibodies. J Clin Microbiol 38: 696–701.
-
23.
Martin DA, Muth DA, Brown T, Johnson AJ, Karabatsos N, Roehrig JT, 2000. Standardization of immunoglobulin M capture enzyme-linked immunosorbent assays for routine diagnosis of arboviral infections. J Clin Microbiol 38: 1823–1826.
-
24.
CDC, 2010. Notes from the field: dengue epidemic—Puerto Rico, January–July 2010. MMWR 59: 878.
-
25.
Ndao M, Spithill TW, Caffrey R, Li H, Podust VN, Perichon R, Santamaria C, Ache A, Duncan M, Powell MR, Ward BJ, 2010. Identification of novel diagnostic serum biomarkers for Chagas' disease in asymptomatic subjects by mass spectrometric profiling. J Clin Microbiol 48: 1139–1149.
-
26.
Gassmann M, Grenacher B, Rohde B, Vogel J, 2009. Quantifying Western blots: pitfalls of densitometry. Electrophoresis 30: 1845–1855.
-
27.
Murphy BR, Whitehead SS, 2011. Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol 29: 587–619.
-
28.
Ray S, Srivastava R, Tripathi K, Vaibhav V, Patankar S, Srivastava S, 2012. Serum poteome changes in dengue virus-infected patients from a dengue-endemic area of India: towards new molecular targets? OMICS 16: 527–536.
-
29.
Sun JF, Shi ZX, Guo HC, Li S, Tu CC, 2011. Proteomic analysis of swine serum following highly virulent classical swine fever virus infection. Virol J 8: 107.
-
30.
Seiffert D, Schleef RR, 1996. Two functionally distinct pools of vitronectin (Vn) in the blood circulation: identification of a heparin-binding competent population of Vn within platelet alpha-granules. Blood 88: 552–560.
-
31.
Preissner KT, Reuning U, 2011. Vitronectin in vascular context: facets of a multitalented matricellular protein. Semin Thromb Hemost 37: 408–424.
-
32.
Izumi M, Yamada KM, Hayashi M, 1989. Vitronectin exists in two structurally and functionally distinct forms in human plasma. Biochim Biophys Acta 990: 101–108.
-
33.
Stefansson S, Haudenschild CC, Lawrence DA, 1998. Beyond fibrinolysis: the role of plasminogen activator inhibitor-1 and vitronectin in vascular wound healing. Trends Cardiovasc Med 8: 175–180.
-
34.
van Aken BE, Seiffert D, Thinnes T, Loskutoff DJ, 1997. Localization of vitronectin in the normal and atherosclerotic human vessel wall. Histochem Cell Biol 107: 313–320.
-
35.
Liu Z, Han Q, Zhang L, Zhao Q, Chen J, Lou S, 2009. Low levels of serum vitronectin associated with clinical phases in patients with hemorrhagic fever with renal syndrome. Clin Exp Med 9: 297–301.
-
36.
Conlan MG, Tomasini BR, Schultz RL, Mosher DF, 1988. Plasma vitronectin polymorphism in normal subjects and patients with disseminated intravascular coagulation. Blood 72: 185–190.
-
37.
Minor KH, Peterson CB, 2002. Plasminogen activator inhibitor type 1 promotes the self-association of vitronectin into complexes exhibiting altered incorporation into the extracellular matrix. J Biol Chem 277: 10337–10345.
-
38.
Akama T, Yamada KM, Seno N, Matsumoto I, Kono I, Kashiwagi H, Funaki T, Hayashi M, 1986. Immunological characterization of human vitronectin and its binding to glycosaminoglycans. J Biochem 100: 1343–1351.
-
39.
Chen Y, Maguire T, Hileman RE, Fromm JR, Esko JD, Linhardt RJ, Marks RM, 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3: 866–871.
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