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Underrecognition of Dengue during 2013 Epidemic in Luanda, Angola - Volume 21, Number 8—August 2015 - Emerging Infectious Disease journal - CDC

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Underrecognition of Dengue during 2013 Epidemic in Luanda, Angola - Volume 21, Number 8—August 2015 - Emerging Infectious Disease journal - CDC

Volume 21, Number 8—August 2015


Underrecognition of Dengue during 2013 Epidemic in Luanda, Angola

Tyler M. SharpComments to Author , Rosa Moreira, Maria José Soares, Lúis Miguel da Costa, Jennifer Mann, Mark DeLorey, Elizabeth Hunsperger, Jorge L. Muñoz-Jordán, Candimar Colón, Harold S. Margolis, Adelaide de Caravalho, and Kay M. Tomashek
Author affiliations: Centers for Disease Control and Prevention, San Juan, Puerto Rico, USA (T.M. Sharp, E. Hunsperger, J.L. Muñoz-Jordán, C. Colón, H.S. Margolis, K.M. Tomashek)Field Epidemiology and Laboratory Training Program–Centers for Disease Control and Prevention, Luanda, Angola (R. Moreira)Ministry of Health of Angola, Luanda (M.S. Soares, L.M. da Costa, A. de Caravalho)Center for Global Health–Centers for Disease Control and Prevention, Luanda (J. Mann)Centers for Disease Control and Prevention, Fort Collins, Colorado, USA (M. DeLorey)


During the 2013 dengue epidemic in Luanda, Angola, 811 dengue rapid diagnostic test–positive cases were reported to the Ministry of Health. To better understand the magnitude of the epidemic and identify risk factors for dengue virus (DENV) infection, we conducted cluster surveys around households of case-patients and randomly selected households 6 weeks after the peak of the epidemic. Of 173 case cluster participants, 16 (9%) exhibited evidence of recent DENV infection. Of 247 random cluster participants, 25 (10%) had evidence of recent DENV infection. Of 13 recently infected participants who had a recent febrile illness, 7 (54%) had sought medical care, and 1 (14%) was hospitalized with symptoms consistent with severe dengue; however, none received a diagnosis of dengue. Behavior associated with protection from DENV infection included recent use of mosquito repellent or a bed net. These findings suggest that the 2013 dengue epidemic was larger than indicated by passive surveillance data.
Dengue is a potentially fatal acute febrile illness caused by any of 4 mosquito-transmitted dengue viruses (DENV-1–4). The disease is endemic throughout the tropics (1), but is underrecognized in sub-Saharan Africa (2,3), where an estimated 64 million DENV infections occurred in 2010 (4). Although dengue was identified in travelers returning from Angola in the 1980s (5), locally acquired cases had not been reported until an outbreak in 2013 that was initially thought to have resulted from importation of DENV by immigrant workers from Asia. However, the only virus detected during the outbreak was a strain of DENV-1 that molecular epidemiologic analysis indicated had been circulating in western and west-central Africa for roughly 4 decades (69), demonstrating regional endemicity of dengue.
During the 2013 epidemic, the Angola Ministry of Health was notified of a total of 1,214 dengue case-patients, nearly all (98%) of whom resided in the capital, Luanda, which has an estimated population of 3–14 million (Angola Ministry of Health and World Health Organization, unpub. data). Serum specimens from suspected cases were tested with a dengue rapid diagnostic test (RDT; SD BIOLINE Dengue Duo, Standard Diagnostics, Haryana, India), and positive cases were defined by detection of nonstructural protein 1 antigen, anti-DENV IgM, or both. In total, specimens from 811 (67%) persons with suspected dengue tested RDT-positive, including those from 246 (30%) hospitalized patients and from 11 (1.4%) patients who died. The highest weekly incidence occurred during May 17–23, 2013, when 125 cases were reported, of which 101 (81%) were RDT-positive.
Dengue is a focal disease, and cases frequently cluster around the households of infected persons (10,11). Previous household-based cluster investigations in Indonesia (12), Nicaragua (13), Thailand (14), and Vietnam (15) demonstrated DENV infection rates of 2.2%–12.4% among persons residing within 10–100 m of index case-patients. These studies enabled detection of unrecognized dengue cases and identification of household risk factors for DENV infection, such as the presence of uncovered water storage containers (12) and lack of piped household water supply (14). Household-based cluster investigations are therefore a useful tool to estimate the extent of dengue in regions where case reporting may be suboptimal and can also facilitate identification of local risk factors for DENV infection.
Dr. Sharp is a lieutenant commander in the US Public Health Service and a health scientist at CDC Dengue Branch in San Juan, Puerto Rico. His research and public health interests include the epidemiology and pathobiology of dengue and other tropical acute febrile illnesses.


We thank Isabel Joao for assistance with field investigation logistics, Victor Luteganya for assistance with data management, Sheryl Shapiro and Jacqueline Weaver for assistance with specimen shipment, Laura Wright for assistance with map creation, and Ray A. Arthur and Serena Fuller for outbreak response support and coordination.
We acknowledge the CDC Global Disease Detection Operations Center Outbreak Response Contingency Fund for financial support of the field investigation.


  1. World Health Organization. Dengue: guidelines for diagnosis, treatment, prevention and control. Geneva: The Organization; 2009.
  2. Amarasinghe AKuritsk JNLetson GWMargolis HSDengue virus infection in Africa. Emerg Infect Dis2011;17:134954 .PubMed
  3. Jaenisch TJunghanss TWills BBrady OJEckerle IFarlow ADengue expansion in Africa-not recognized or not happening? Emerg Infect Dis.2014;20:•••DOIPubMed
  4. Bhatt SGething PWBrady OJMessina JPFarlow AWMoyes CLThe global distribution and burden of dengue. Nature2013;496:5047.DOIPubMed
  5. Bakker RCVeenstra JDingemans-Dumas AMWetsteyn JKager PAImported dengue in the Netherlands. J Travel Med1996;3:2048.DOIPubMed
  6. Schwartz EMeltzer EMendelson MTooke ASteiner FGautret PDetection on four continents of dengue fever cases related to an ongoing outbreak in Luanda, Angola, March to May 2013. Euro Surveill2013;18:20488 .PubMed
  7. Sessions OMKhan KHou YMeltzer EQuam MSchwartz EExploring the origin and potential for spread of the 2013 dengue outbreak in Luanda, Angola. Glob Health Action. 2013;6:218–22.
  8. Centers for Disease Control and PreventionOngoing dengue epidemic—Angola, June 2013. MMWR Morb Mortal Wkly Rep2013;62:5047.PubMed
  9. Parreira RConceicao CCenteno-Lima SMarques NSaraiva da Cunha JAbreu CAngola’s 2013 dengue outbreak: clinical, laboratory and molecular analyses of cases from four Portuguese institutions. J Infect Dev Ctries2014;8:12105DOIPubMed
  10. Morrison ACGetis ASantiago MRigau-Perez JGReiter PExploratory space-time analysis of reported dengue cases during an outbreak in Florida, Puerto Rico, 1991–1992. Am J Trop Med Hyg1998;58:28798 .PubMed
  11. Salje HLessler JEndy TPCurriero FCGibbons RVNisalak ARevealing the microscale spatial signature of dengue transmission and immunity in an urban population. Proc Natl Acad Sci U S A2012;109:95358DOIPubMed
  12. Beckett CGKosasih HFaisal I. Nurhayati, Tan R, Widjaja S, et al. Early detection of dengue infections using cluster sampling around index cases. Am J Trop Med Hyg. 2005;72:777–82.
  13. Reyes MMercado JCStandish KMatute JCOrtega OMoraga BIndex cluster study of dengue virus infection in Nicaragua. Am J Trop Med Hyg.2010;83:6839DOIPubMed
  14. Mammen MPPimgate CKoenraadt CJRothman ALAldstadt JNisalak ASpatial and temporal clustering of dengue virus transmission in Thai villages. PLoS Med2008;5:e205DOIPubMed
  15. Anders KLNga LHThuy NTNgoc TVTam CTTai LTHouseholds as foci for dengue transmission in highly urban Vietnam. PLoS Negl Trop Dis.2015;9:e0003528DOIPubMed
  16. Santiago GAVergne EQuiles YCosme JVazquez JMedina JFAnalytical and clinical performance of the CDC real time RT-PCR assay for detection and typing of dengue virus. PLoS Negl Trop Dis2013;7:e2311DOIPubMed
  17. Miagostovich MPNogueira RMdos Santos FBSchatzmayr HGAraujo ESVorndam VEvaluation of an IgG enzyme-linked immunosorbent assay for dengue diagnosis. J Clin Virol1999;14:1839DOIPubMed
  18. Ellis EMNeatherlin JCDelorey MOchieng MMohammed AHMogeni DOA household aerosurvey to estimate the magnitude of a dengue outbreak in Mombasa, Kenya, 2013. PLoS Negl Trop Dis2015;9:e0003733 . DOIPubMed
  19. Sharp TMHunsperger ESantiago GAMunoz-Jordan JLSantiago LMRivera AVirus-specific differences in rates of disease during the 2010 dengue epidemic in Puerto Rico. PLoS Negl Trop Dis2013;7:e2159DOIPubMed
  20. Villar LARojas DPBesada-Lombana SSarti EEpidemiological trends of dengue disease in Colombia (2000–2011): a systematic review. PLoS Negl Trop Dis2015;9:e0003499DOIPubMed
  21. Teixeira MGSiqueira JB JrFerreira GLBricks LJoint GEpidemiological trends of dengue disease in Brazil (2000–2010): a systematic literature search and analysis. PLoS Negl Trop Dis2013;7:e2520DOIPubMed
  22. Stoler JAl Dashti RAnto FFobil JNAwandare GADeconstructing “malaria”: West Africa as the next front for dengue fever surveillance and control. Acta Trop2014;134:5865DOIPubMed
  23. Stoler JDelimini RKBonney JHOduro AROwusu-Agyei SFobil JNEvidence of recent dengue exposure among malaria parasite-positive children in three urban centers in Ghana. Am J Trop Med Hyg2015;92:497500 . DOIPubMed
  24. Crump JAMorrissey ABNicholson WLMassung RFStoddard RAGalloway RLEtiology of severe non-malaria febrile illness in northern Tanzania: a prospective cohort study. PLoS Negl Trop Dis2013;7:e2324DOIPubMed
  25. Thwing JIMihigo JFernandes APSaute FFerreira CFortes FHow much malaria occurs in urban Luanda, Angola? A health facility-based assessment. Am J Trop Med Hyg2009;80:48791 .PubMed
  26. Stoddard STForshey BMMorrison ACPaz-Soldan VAVazquez-Prokopec GMAstete HHouse-to-house human movement drives dengue virus transmission. Proc Natl Acad Sci U S A2013;110:9949DOIPubMed
  27. Yoon IKGetis AAldstadt JRothman ALTannitisupawong DKoenraadt CJFine scale spatiotemporal clustering of dengue virus transmission in children and Aedes aegypti in rural Thai villages. PLoS Negl Trop Dis. 2012;6:e1730. PMID: 22816001
  28. Cummings DAIrizarry RAHuang NEEndy TPNisalak AUngchusak KTravelling waves in the occurrence of dengue haemorrhagic fever in Thailand. Nature2004;427:3447DOIPubMed
  29. Sharp TWWallace MRHayes CGSanchez JLDeFraites RFArthur RRDengue fever in US troops during Operation Restore Hope, Somalia, 1992–1993. Am J Trop Med Hyg1995;53:8994 .PubMed
  30. Chadee DDCorbet PSA night-time role of the oviposition site of the mosquito, Aedes aegypti (L.) (Diptera: Culicidae). Ann Trop Med Parasitol.1990;84:42933 .PubMed
  31. Harrington LCPonlawat AEdman JDScott TWVermeylen FInfluence of container size, location, and time of day on oviposition patterns of the dengue vector, Aedes aegypti, in Thailand. Vector Borne Zoonotic Dis2008;8:41523DOIPubMed
  32. Calisher CHKarabatsos NDalrymple JMShope REPorterfield JSWestaway EGAntigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol1989;70:3743DOIPubMed
  33. Parreira RCenteno-Lima SLopes APortugal-Calisto DConstantino ANina JDengue virus serotype 4 and chikungunya virus coinfection in a traveller returning from Luanda, Angola. Euro Surveill2014;19:20730 .PubMed
  34. Meltzer ELustig YGlichinsky OSteiner FSchwartz EProbable importation of dengue virus type 4 to Angola from Brazil. Emerg Infect Dis.2014;20:17756DOIPubMed
  35. Lam PKTam DTDiet TVTam CTTien NTKieu NTClinical characteristics of dengue shock syndrome in Vietnamese children: a 10-year prospective study in a single hospital. Clin Infect Dis2013;57:157786DOIPubMed
  36. Teixeira MGAndrade AMCosta Mda CCastro JNOliveira FLGoes CSEast/Central/South African genotype chikungunya virus, Brazil, 2014.Emerg Infect Dis2015;21:9067 PubMedDOIPubMed



Suggested citation for this article: Sharp TM, Moreira R, Soares MJ, da Costa LM, Mann J, DeLorey M, et al. Underrecognition of dengue during 2013 epidemic in Luanda, Angola. Emerg Infect Dis. 2015 Aug [date cited].
DOI: 10.3201/eid2108.150368

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