Distribution of Dengue Virus Types 1 and 4 in Blood Components from Infected Blood Donors from Puerto Rico
Abstract
Dengue is a mosquito-borne viral disease caused by the four dengue viruses (DENV-1 to 4) that can also be transmitted by blood transfusion and organ transplantation. The distribution of DENV in the components of blood from infected donors is poorly understood. Here, we used an in-house TaqMan qRT-PCR assay to test residual samples of plasma, cellular components of whole blood (CCWB), serum and clot specimens from the same collection from blood donors who were DENV-RNA-reactive in a parallel blood safety study. To assess whether DENV RNA detected by TaqMan was associated with infectious virus, DENV infectivity in available samples was determined by culture in mosquito cells. As a result, DENV RNA was detected by TaqMan in all tested blood components, albeit more consistently in the cellular components; 78.8% of CCWB, 73.3% of clots, 86.7% of sera and 41.8% of plasma samples. DENV-1 was detected in 48 plasma and 97 CCWB samples while DENV-4 was detected in 21 plasma and 31 CCWB samples. In mosquito cell cultures, 29/111 (26.1%) plasma and 32/97 (32.7%) CCWB samples were infectious. A subset of samples from 29 donors was separately analyzed to compare DENV viral loads in the available blood components. DENV viral loads didmore »
- Authors:
-
- U.S. Food and Drug Administration, Silver Springs, MD (United States); Sanofi Pasteur, Swiftwater, PA (United States)
- U.S. Food and Drug Administration, Silver Springs, MD (United States); Virginia Commonwealth Univ., Richmond, VA (United States)
- U.S. Food and Drug Administration, Silver Springs, MD (United States)
- U.S. Food and Drug Administration, Silver Springs, MD (United States); Univ. del Zulia, Maracaibo (Venezuela)
- U.S. Food and Drug Administration, Silver Springs, MD (United States); Fundacao Oswaldo Cruz-FIOCRUZ, Rio de Janeiro (Brazil)
- U.S. Food and Drug Administration, Silver Springs, MD (United States); Centro de Pesquisas Rene Rachou, Minas Gerais (Brazil)
- American Red Cross, Gaithersburg, MD (United States)
- Duke-NUS GMS (Singapore)
- Publication Date:
- Research Org.:
- Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1376847
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Neglected Tropical Diseases (Online)
- Additional Journal Information:
- Journal Name: PLoS Neglected Tropical Diseases (Online); Journal Volume: 10; Journal Issue: 2; Journal ID: ISSN 1935-2735
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; blood plasma; blood; viral load; RNA extraction; blood donors; West Nile virus; plasma cells; dengue virus
Citation Formats
Anez, German, Heisey, Daniel A. R., Chancey, Caren, Fares, Rafaelle C. G., Espina, Luz M., Souza, Katia P. R., Teixeira-Carvalho, Andrea, Krysztof, David E., Foster, Gregory A., Stramer, Susan L., Rios, Maria, and Gubler, Duane J. Distribution of Dengue Virus Types 1 and 4 in Blood Components from Infected Blood Donors from Puerto Rico. United States: N. p., 2016.
Web. doi:10.1371/journal.pntd.0004445.
Anez, German, Heisey, Daniel A. R., Chancey, Caren, Fares, Rafaelle C. G., Espina, Luz M., Souza, Katia P. R., Teixeira-Carvalho, Andrea, Krysztof, David E., Foster, Gregory A., Stramer, Susan L., Rios, Maria, & Gubler, Duane J. Distribution of Dengue Virus Types 1 and 4 in Blood Components from Infected Blood Donors from Puerto Rico. United States. https://doi.org/10.1371/journal.pntd.0004445
Anez, German, Heisey, Daniel A. R., Chancey, Caren, Fares, Rafaelle C. G., Espina, Luz M., Souza, Katia P. R., Teixeira-Carvalho, Andrea, Krysztof, David E., Foster, Gregory A., Stramer, Susan L., Rios, Maria, and Gubler, Duane J. Fri .
"Distribution of Dengue Virus Types 1 and 4 in Blood Components from Infected Blood Donors from Puerto Rico". United States. https://doi.org/10.1371/journal.pntd.0004445. https://www.osti.gov/servlets/purl/1376847.
@article{osti_1376847,
title = {Distribution of Dengue Virus Types 1 and 4 in Blood Components from Infected Blood Donors from Puerto Rico},
author = {Anez, German and Heisey, Daniel A. R. and Chancey, Caren and Fares, Rafaelle C. G. and Espina, Luz M. and Souza, Katia P. R. and Teixeira-Carvalho, Andrea and Krysztof, David E. and Foster, Gregory A. and Stramer, Susan L. and Rios, Maria and Gubler, Duane J.},
abstractNote = {Dengue is a mosquito-borne viral disease caused by the four dengue viruses (DENV-1 to 4) that can also be transmitted by blood transfusion and organ transplantation. The distribution of DENV in the components of blood from infected donors is poorly understood. Here, we used an in-house TaqMan qRT-PCR assay to test residual samples of plasma, cellular components of whole blood (CCWB), serum and clot specimens from the same collection from blood donors who were DENV-RNA-reactive in a parallel blood safety study. To assess whether DENV RNA detected by TaqMan was associated with infectious virus, DENV infectivity in available samples was determined by culture in mosquito cells. As a result, DENV RNA was detected by TaqMan in all tested blood components, albeit more consistently in the cellular components; 78.8% of CCWB, 73.3% of clots, 86.7% of sera and 41.8% of plasma samples. DENV-1 was detected in 48 plasma and 97 CCWB samples while DENV-4 was detected in 21 plasma and 31 CCWB samples. In mosquito cell cultures, 29/111 (26.1%) plasma and 32/97 (32.7%) CCWB samples were infectious. A subset of samples from 29 donors was separately analyzed to compare DENV viral loads in the available blood components. DENV viral loads did not differ significantly between components and ranged from 3–8 log10 PCR-detectable units/ml. In conclusion, DENV was present in all tested components from most donors, and viral RNA was not preferentially distributed in any of the tested components. Infectious DENV was also present in similar proportions in cultured plasma, clot and CCWB samples, indicating that these components may serve as a resource when sample sizes are limited. However, these results suggest that the sensitivity of the nucleic acid tests (NAT) for these viruses would not be improved by testing whole blood or components other than plasma.},
doi = {10.1371/journal.pntd.0004445},
journal = {PLoS Neglected Tropical Diseases (Online)},
number = 2,
volume = 10,
place = {United States},
year = {Fri Feb 12 00:00:00 EST 2016},
month = {Fri Feb 12 00:00:00 EST 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 8 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Dengue in Travelers: Kinetics of Viremia and NS1 Antigenemia and Their Associations with Clinical Parameters
journal, June 2013
- Erra, Elina O.; Korhonen, Essi M.; Voutilainen, Liina
- PLoS ONE, Vol. 8, Issue 6
Dengue Hemorrhagic Fever Transmitted by Blood Transfusion
journal, October 2008
- Tambyah, Paul A.; Koay, Evelyn S. C.; Poon, Michelle L. M.
- New England Journal of Medicine, Vol. 359, Issue 14
Epidemiological Risk Factors Associated with High Global Frequency of Inapparent Dengue Virus Infections
journal, June 2014
- Grange, Laura; Simon-Loriere, Etienne; Sakuntabhai, Anavaj
- Frontiers in Immunology, Vol. 5
Kinetics of Viremia and NS1 Antigenemia Are Shaped by Immune Status and Virus Serotype in Adults with Dengue
journal, September 2011
- Tricou, Vianney; Minh, Nguyet Nguyen; Farrar, Jeremy
- PLoS Neglected Tropical Diseases, Vol. 5, Issue 9
Collaborative study to evaluate a working reagent for West Nile virus RNA detection by nucleic acid testing
journal, January 2005
- Saldanha, John; Shead, Susan; Heath, Alan
- Transfusion, Vol. 45, Issue 1
West Nile Virus RNA in Tissues from Donor Associated with Transmission to Organ Transplant Recipients
journal, September 2013
- Blau, Dianna M.; Rabe, Ingrid B.; Bhatnagar, Julu
- Emerging Infectious Diseases, Vol. 19, Issue 9
Dengue virus and other arboviruses: a global view of risks: Risks of dengue and other arboviruses
journal, June 2012
- Anez, G.; Chancey, C.; Grinev, A.
- ISBT Science Series, Vol. 7, Issue 1
Global spread of dengue virus types: mapping the 70 year history
journal, March 2014
- Messina, Jane P.; Brady, Oliver J.; Scott, Thomas W.
- Trends in Microbiology, Vol. 22, Issue 3
Rare and Emerging Viral Infections in Transplant Recipients
journal, July 2013
- Waggoner, J. J.; Soda, E. A.; Deresinski, S.
- Clinical Infectious Diseases, Vol. 57, Issue 8
Differing Influences of Virus Burden and Immune Activation on Disease Severity in Secondary Dengue‐3 Virus Infections
journal, May 2002
- Libraty, Daniel H.; Endy, Timothy P.; Houng, Huo‐Shu H.
- The Journal of Infectious Diseases, Vol. 185, Issue 9
Virus-Specific Differences in Rates of Disease during the 2010 Dengue Epidemic in Puerto Rico
journal, April 2013
- Sharp, Tyler M.; Hunsperger, Elizabeth; Santiago, Gilberto A.
- PLoS Neglected Tropical Diseases, Vol. 7, Issue 4
Estimated prevalence of dengue viremia in Puerto Rican blood donations, 1995 through 2010: PREVALENCE OF DENGUE VIREMIC DONATIONS
journal, February 2012
- Petersen, Lyle R.; Tomashek, Kay M.; Biggerstaff, Brad J.
- Transfusion, Vol. 52, Issue 8
Serotype-Specific Detection of Dengue Viruses in a Fourplex Real-Time Reverse Transcriptase PCR Assay
journal, October 2005
- Johnson, B. W.; Russell, B. J.; Lanciotti, R. S.
- Journal of Clinical Microbiology, Vol. 43, Issue 10
The global distribution and burden of dengue
journal, April 2013
- Bhatt, Samir; Gething, Peter W.; Brady, Oliver J.
- Nature, Vol. 496, Issue 7446
Real-time symptomatic case of transfusion-transmitted dengue: DENGUE TRANSMISSION BY TRANSFUSION
journal, January 2015
- Levi, José Eduardo; Nishiya, Anna; Félix, Alvina Clara
- Transfusion, Vol. 55, Issue 5
Dengue in the United States of America: A Worsening Scenario?
journal, January 2013
- Añez, Germán; Rios, Maria
- BioMed Research International, Vol. 2013
West Nile virus nucleic acid persistence in whole blood months after clearance in plasma: implication for transfusion and transplantation safety: WNV RNA Persistence in Whole Blood
journal, June 2014
- Lanteri, Marion C.; Lee, Tzong-Hae; Wen, Li
- Transfusion, Vol. 54, Issue 12
Dengue and dengue vectors in the WHO European region: past, present, and scenarios for the future
journal, December 2014
- Schaffner, Francis; Mathis, Alexander
- The Lancet Infectious Diseases, Vol. 14, Issue 12
Transmission of dengue virus from a donor to a recipient after living donor liver transplantation: Letter to the Editors
journal, October 2013
- Saigal, Sanjiv; Choudhary, Narendra S.; Saraf, Neeraj
- Liver Transplantation, Vol. 19, Issue 12
Establishment of the First International Standard for Nucleic Acid Amplification Technology (NAT) Assays for HCV RNA
journal, April 1999
- Saldanha, J.; Lelie, N.; Heath, A.
- Vox Sanguinis, Vol. 76, Issue 3
Dengue Virus Transmission by Blood Stem Cell Donor after Travel to Sri Lanka; Germany, 2013
journal, August 2014
- Punzel, Michael; Korukluoğlu, Gülay; Caglayik, Dilek Yagci
- Emerging Infectious Diseases, Vol. 20, Issue 8
Bitten by a bug or a bag? Transfusion-transmitted dengue: a rare complication in the bleeding surgical patient: Dengue Transmission From A Blood Transfusion
journal, February 2015
- Oh, Han Boon; Muthu, Vaishnavi; Daruwalla, Zubin J.
- Transfusion, Vol. 55, Issue 7
Dengue virus in blood donations, Puerto Rico, 2005
journal, July 2008
- Mohammed, Hamish; Linnen, Jeffrey M.; Muoz-Jordn, Jorge L.
- Transfusion, Vol. 48, Issue 7
Dengue viremia in blood donors identified by RNA and detection of dengue transfusion transmission during the 2007 dengue outbreak in Puerto Rico: DENGUE TRANSFUSION TRANSMISSION
journal, February 2012
- Stramer, Susan L.; Linnen, Jeffrey M.; Carrick, James M.
- Transfusion, Vol. 52, Issue 8
Phylogenetic Analysis of Dengue Virus Types 1 and 4 Circulating in Puerto Rico and Key West, Florida, during 2010 Epidemics
journal, September 2012
- Rios, Maria; Stramer, Susan L.; Añez, Germán
- The American Journal of Tropical Medicine and Hygiene, Vol. 87, Issue 3
Detection of dengue virus in sera of Brazilian blood donors: DENGUE VIRUS IN SERA OF BLOOD DONORS
journal, June 2012
- Dias, Leny Lobo; Amarilla, Alberto Anastacio; Poloni, Telma Regina
- Transfusion, Vol. 52, Issue 8
High Levels of Plasma Dengue Viral Load during Defervescence in Patients with Dengue Hemorrhagic Fever: Implications for Pathogenesis
journal, January 2003
- Wang, Wei-Kung; Chao, Day-Yu; Kao, Chuan-Liang
- Virology, Vol. 305, Issue 2
Relative distribution of West Nile virus RNA in blood compartments: implications for blood donor nucleic acid amplification technology screening: WNV RNA IN BLOOD COMPARTMENTS
journal, August 2011
- Lai, Lori; Lee, Tzong-Hae; Tobler, Leslie
- Transfusion, Vol. 52, Issue 2
Prevalence of anti-dengue immunoglobulin G antibodies among American Red Cross blood donors in Puerto Rico, 2006: DENGUE VIRUS ANTIBODIES IN BLOOD DONORS
journal, January 2012
- Mohammed, Hamish; Tomashek, Kay M.; Stramer, Susan L.
- Transfusion, Vol. 52, Issue 8
Severe Nonfebrile Dengue Infection in an Adolescent After Postoperative Kidney Transplantation: A Case Report
journal, January 2012
- Tangnararatchakit, K.; Tirapanich, W.; Tapaneya-Olarn, W.
- Transplantation Proceedings, Vol. 44, Issue 1
Dengue viremia in blood donors from Honduras, Brazil, and Australia
journal, July 2008
- Linnen, Jeffrey M.; Vinelli, Elizabeth; Sabino, Ester C.
- Transfusion, Vol. 48, Issue 7
Travel-associated infection presenting in Europe (2008–12): an analysis of EuroTravNet longitudinal, surveillance data, and evaluation of the effect of the pre-travel consultation
journal, January 2015
- Schlagenhauf, Patricia; Weld, Leisa; Goorhuis, Abraham
- The Lancet Infectious Diseases, Vol. 15, Issue 1
Rapid focus reduction neutralization test of Japanese encephalitis virus in microtiter system
journal, March 1985
- Okuno, Y.; Fukunaga, T.; Tadano, M.
- Archives of Virology, Vol. 86, Issue 1-2
Transfusion Transmitted Infections in Solid Organ Transplantation: Transfusion Infections in Organ Transplants
journal, January 2015
- Mezochow, A. K.; Henry, R.; Blumberg, E. A.
- American Journal of Transplantation, Vol. 15, Issue 2
Dengue Viremia Titer, Antibody Response Pattern, and Virus Serotype Correlate with Disease Severity
journal, January 2000
- Vaughn, David W.; Green, Sharone; Kalayanarooj, Siripen
- The Journal of Infectious Diseases, Vol. 181, Issue 1
West Nile Virus Adheres to Human Red Blood Cells in Whole Blood
journal, July 2007
- Rios, M.; Daniel, S.; Chancey, C.
- Clinical Infectious Diseases, Vol. 45, Issue 2
Distribution of hepatitis C virus in circulating blood components from blood donors: HCV distribution in circulating blood
journal, March 2012
- Chancey, C.; Winkelman, V.; Foley, J. B.
- Vox Sanguinis, Vol. 103, Issue 2
Keeping Blood Transfusion Safe From West Nile Virus: American Red Cross Experience, 2003 to 2012
journal, July 2015
- Dodd, Roger Y.; Foster, Gregory A.; Stramer, Susan L.
- Transfusion Medicine Reviews, Vol. 29, Issue 3
Virus and Antibody Dynamics in Acute West Nile Virus Infection
journal, October 2008
- Busch, Michael P.; Kleinman, Steven H.; Tobler, Leslie H.
- The Journal of Infectious Diseases, Vol. 198, Issue 7
Transmission of dengue virus from a donor to a recipient after living donor liver transplantation: Letter to the Editors
journal, October 2013
- Saigal, Sanjiv; Choudhary, Narendra S.; Saraf, Neeraj
- Liver Transplantation, Vol. 19, Issue 12
Keeping Blood Transfusion Safe From West Nile Virus: American Red Cross Experience, 2003 to 2012
journal, July 2015
- Dodd, Roger Y.; Foster, Gregory A.; Stramer, Susan L.
- Transfusion Medicine Reviews, Vol. 29, Issue 3
Severe Nonfebrile Dengue Infection in an Adolescent After Postoperative Kidney Transplantation: A Case Report
journal, January 2012
- Tangnararatchakit, K.; Tirapanich, W.; Tapaneya-Olarn, W.
- Transplantation Proceedings, Vol. 44, Issue 1
Insights into the epidemiology, natural history and pathogenesis of hepatitis C virus infection from studies of infected donors and blood product recipients
journal, June 2001
- Busch, M. P.
- Transfusion Clinique et Biologique, Vol. 8, Issue 3
Dengue Viremia Titer, Antibody Response Pattern, and Virus Serotype Correlate with Disease Severity
journal, January 2000
- Vaughn, David W.; Green, Sharone; Kalayanarooj, Siripen
- The Journal of Infectious Diseases, Vol. 181, Issue 1
Differing Influences of Virus Burden and Immune Activation on Disease Severity in Secondary Dengue‐3 Virus Infections
journal, May 2002
- Libraty, Daniel H.; Endy, Timothy P.; Houng, Huo‐Shu H.
- The Journal of Infectious Diseases, Vol. 185, Issue 9
West Nile Virus Adheres to Human Red Blood Cells in Whole Blood
journal, July 2007
- Rios, M.; Daniel, S.; Chancey, C.
- Clinical Infectious Diseases, Vol. 45, Issue 2
Virus and Antibody Dynamics in Acute West Nile Virus Infection
journal, October 2008
- Busch, Michael P.; Kleinman, Steven H.; Tobler, Leslie H.
- The Journal of Infectious Diseases, Vol. 198, Issue 7
Rare and Emerging Viral Infections in Transplant Recipients
journal, July 2013
- Waggoner, J. J.; Soda, E. A.; Deresinski, S.
- Clinical Infectious Diseases, Vol. 57, Issue 8
Transfusion Transmitted Infections in Solid Organ Transplantation: Transfusion Infections in Organ Transplants
journal, January 2015
- Mezochow, A. K.; Henry, R.; Blumberg, E. A.
- American Journal of Transplantation, Vol. 15, Issue 2
Collaborative study to evaluate a working reagent for West Nile virus RNA detection by nucleic acid testing
journal, January 2005
- Saldanha, John; Shead, Susan; Heath, Alan
- Transfusion, Vol. 45, Issue 1
Dengue virus in blood donations, Puerto Rico, 2005
journal, July 2008
- Mohammed, Hamish; Linnen, Jeffrey M.; Muoz-Jordn, Jorge L.
- Transfusion, Vol. 48, Issue 7
Dengue viremia in blood donors from Honduras, Brazil, and Australia
journal, July 2008
- Linnen, Jeffrey M.; Vinelli, Elizabeth; Sabino, Ester C.
- Transfusion, Vol. 48, Issue 7
Relative distribution of West Nile virus RNA in blood compartments: implications for blood donor nucleic acid amplification technology screening: WNV RNA IN BLOOD COMPARTMENTS
journal, August 2011
- Lai, Lori; Lee, Tzong-Hae; Tobler, Leslie
- Transfusion, Vol. 52, Issue 2
Prevalence of anti-dengue immunoglobulin G antibodies among American Red Cross blood donors in Puerto Rico, 2006: DENGUE VIRUS ANTIBODIES IN BLOOD DONORS
journal, January 2012
- Mohammed, Hamish; Tomashek, Kay M.; Stramer, Susan L.
- Transfusion, Vol. 52, Issue 8
Estimated prevalence of dengue viremia in Puerto Rican blood donations, 1995 through 2010: PREVALENCE OF DENGUE VIREMIC DONATIONS
journal, February 2012
- Petersen, Lyle R.; Tomashek, Kay M.; Biggerstaff, Brad J.
- Transfusion, Vol. 52, Issue 8
West Nile virus nucleic acid persistence in whole blood months after clearance in plasma: implication for transfusion and transplantation safety: WNV RNA Persistence in Whole Blood
journal, June 2014
- Lanteri, Marion C.; Lee, Tzong-Hae; Wen, Li
- Transfusion, Vol. 54, Issue 12
Bitten by a bug or a bag? Transfusion-transmitted dengue: a rare complication in the bleeding surgical patient: Dengue Transmission From A Blood Transfusion
journal, February 2015
- Oh, Han Boon; Muthu, Vaishnavi; Daruwalla, Zubin J.
- Transfusion, Vol. 55, Issue 7
Virus-Specific Differences in Rates of Disease during the 2010 Dengue Epidemic in Puerto Rico
journal, April 2013
- Sharp, Tyler M.; Hunsperger, Elizabeth; Santiago, Gilberto A.
- PLoS Neglected Tropical Diseases, Vol. 7, Issue 4
Dengue in Travelers: Kinetics of Viremia and NS1 Antigenemia and Their Associations with Clinical Parameters
journal, June 2013
- Erra, Elina O.; Korhonen, Essi M.; Voutilainen, Liina
- PLoS ONE, Vol. 8, Issue 6
West Nile Virus RNA in Tissues from Donor Associated with Transmission to Organ Transplant Recipients
journal, September 2013
- Blau, Dianna M.; Rabe, Ingrid B.; Bhatnagar, Julu
- Emerging Infectious Diseases, Vol. 19, Issue 9
Dengue Virus Transmission by Blood Stem Cell Donor after Travel to Sri Lanka; Germany, 2013
journal, August 2014
- Punzel, Michael; Korukluoğlu, Gülay; Caglayik, Dilek Yagci
- Emerging Infectious Diseases, Vol. 20, Issue 8
Phylogenetic Analysis of Dengue Virus Types 1 and 4 Circulating in Puerto Rico and Key West, Florida, during 2010 Epidemics
journal, September 2012
- Rios, Maria; Stramer, Susan L.; Añez, Germán
- The American Journal of Tropical Medicine and Hygiene, Vol. 87, Issue 3
Works referencing / citing this record:
A smartphone-based diagnostic platform for rapid detection of Zika, chikungunya, and dengue viruses
journal, March 2017
- Priye, Aashish; Bird, Sara W.; Light, Yooli K.
- Scientific Reports, Vol. 7, Issue 1
Pathogen inactivation of Dengue virus in red blood cells using amustaline and glutathione: DENGUE VIRUS INACTIVATION IN RBCs BY AMUSTALINE
journal, September 2017
- Aubry, Maite; Laughhunn, Andrew; Santa Maria, Felicia
- Transfusion, Vol. 57, Issue 12
Identification and characterization of permissive cells to dengue virus infection in human hematopoietic stem and progenitor cells
journal, May 2019
- Hsu, Alan Y.; Ho, Tzu‐Chuan; Lai, Mei‐Ling
- Transfusion, Vol. 59, Issue 9
Cost of illness and program of dengue: A systematic review
journal, February 2019
- Oliveira, Luana Nice da Silva; Itria, Alexander; Lima, Erika Coutinho
- PLOS ONE, Vol. 14, Issue 2
The prevalence of dengue virus serotypes in asymptomatic blood donors reveals the emergence of serotype 4 in Saudi Arabia
journal, June 2017
- Ashshi, Ahmed Mohamed
- Virology Journal, Vol. 14, Issue 1
Cost of illness and program of dengue: A systematic review
journal, February 2019
- Oliveira, Luana Nice da Silva; Itria, Alexander; Lima, Erika Coutinho
- PLOS ONE, Vol. 14, Issue 2