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Probable Importation of Dengue Virus Type 4 to Angola from Brazil LETTERS Probable Angola and who were hospitalized (http://doua.prabi.fr/software/njplot). within days of returning to their home Results showed that RNA from this Importation of countries because of signs and symp- isolate was most closely related to Dengue Virus toms of dengue fever. None of the that of a DENV-4 strain identified in Type 4 to Angola case-patients met criteria for severe 2010 in Boa Vista, the capital of Ro- dengue, and all recovered unevent- raima State in the Amazon Region of from Brazil fully. Acute DENV infection was Brazil (7) (Figure). To the Editor: The prevalence confirmed by serologic testing in all DENV-4 infection was previ- of dengue virus (DENV) infection in 3 patients and by positive results for a ously reported in Africa in 1986, when Africa may have been grossly under- nonstructural protein 1 serum antigen 2 cases were identified in travelers estimated for many years (1). Even test in 2 travelers. returning from Senegal (8), but to though published reports are scarce, In a serum sample taken from 1 our knowledge, no other cases have dengue has been documented in at of the travelers from Israel on the sec- been reported in western or south- least 34 countries in Africa (2). The ond day of fever, DENV RNA was de- western Africa. During the April 2013 role of travelers as sentinels of infec- tected by using reverse transcription dengue outbreak in Luanda, only tious disease has proven to be invalu- PCR. This strain was found to belong DENV-1 was isolated (3,4). After able in this regard; dengue in return- to DENV type 4 (DENV-4). Phylo- that outbreak, a study conducted on ing travelers was the only evidence genetic analysis was performed, and the basis of modeling of international for local DENV transmission for 12 of multiple sequence alignment of this commercial flight data to and from these countries. DENV-4 sequence, in comparison to Angola suggested that DENV would During April 2013, simultaneous other DENV-4 sequences retrieved most likely have been imported from reports of travelers returning from from GenBank, was performed by Latin America (5). Our finding, a year Luanda, Angola, with dengue fever using the Sequencher 5.0 program later, of DENV-4 in Angola that was emerged from Israel, several countries (Gencodes Corporation, Ann Arbor, closely related to strains from Brazil in Europe, Canada, and South Africa; MI, USA). A maximum-likelihood appears to vindicate this modeling PCR and sequencing of viral RNA phylogenetic tree was inferred from system. During the past decade, Bra- confirmed the causative species to be the sequence alignment by using zil had been experiencing a consistent DENV type 1 (DENV-1) (3). Con- ClustalX (http://www.clustal.org), increase in dengue epidemics and in comitantly, a large outbreak of dengue and the robustness of the tree was severity of disease (9). Brazil’s large was confirmed by local authorities in assessed by 1,000 bootstrap replica- and growing economy, its increas- Luanda, and DENV-1 was isolated in tions. The tree was visualized and ingly prominent place in world trade, samples from local residents (4). The produced by using NJ plot software and its growing tourism industry high- origin of the outbreak strain was not ascertained, but phylogenetic analy- sis suggested that it had close affinity with isolates from West Africa (4,5). These reports involved almost 100 travelers and >500 residents of Lu- anda who become within a short time. Active DENV transmission and oc- currence of new cases in Luanda were still ongoing during early July 2013 (6), but since then, to our knowledge, no additional local data on DENV ac- tivity in Luanda have been published. We report 3 new cases of den- gue fever acquired in Luanda dur- Figure. Phylogenetic analysis of a dengue virus (DENV) type 4 strain isolate (boldface) ing December 2013–February 2014. from a patient in Israel who apparently acquired DENV in Angola in 2014, showing close Two cases occurred in travelers who relationship with isolates from Brazil. The DENV isolate was aligned with representative returned to Israel, and 1 occurred in DENV sequences from around the world, representing serotypes 1–4. Reference strains, downloaded from public databases (http://www.ncbi.nlm.nih.gov/nuccore), are identified by a traveler who returned to Germany. accession number, place, and year of isolation (DENV-4 isolates) or by serotype, accession All 3 cases occurred in middle-aged number, and year of isolation (DENV-1–3 isolates). Specific branches indicate bootstrap businessmen who had traveled to values. Scale bar indicates percentage identity difference. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 20, No. 10, October 2014 1775 LETTERS light the country’s potential role in the 5. Sessions OM, Khan K, Hou Y, Meltzer E, Borrelia garinii global circulation of DENV. Quam M, Schwartz E, et al. Exploring the origin and potential for spread of the 2013 and Rickettsia Our findings are corroborated by dengue outbreak in Luanda, Angola. Glob a recently reported case of dengue in Health Action. 2013;6:21822. monacensis in a traveler from Portugal that was ac- 6. ProMed-mail. Dengue—Angola (06), Ixodes ricinus quired in Luanda concomitantly with update [cited 2014 Mar 20]. http://www. promedmail.org, article no. 1824865. Ticks, Algeria our cases and also found to be caused 7. Nunes MR, Faria NR, Vasconcelos HB, by DENV-4 (10). In light of the ap- Medeiros DB, Silva de Lima CP, To the Editor: Lyme disease Carvalho VL, et al. Phylogeography of parent introduction of DENV-4 to (Lyme borreliosis) is caused by a Angola, probably from Brazil, health dengue virus serotype 4, Brazil, 2010–2011. Emerg Infect Dis. 2012;18:1858–64. http:// group of related spirochetes (Borrelia authorities should be encouraged to dx.doi.org/10.3201/eid1811.120217 burgdorferi sensu lato) that include enhance surveillance and vector con- 8. Saluzzo JF, Cornet M, Castagnet P, ≥11 species (1). In northern Africa, Rey C, Digoutte JP. Isolation of den- trol efforts. In addition, health prac- the main vector of Lyme disease in titioners treating travelers returning gue 2 and dengue 4 viruses from pa- tients in Senegal. Trans R Soc Trop Europe (Ixodes ricinus ticks) is also from Angola should be aware of the Med Hyg. 1986;80:5. http://dx.doi. present, and this disease has been sus- risk for DENV infection. org/10.1016/0035-9203(86)90182-3 pected to be present in this region of 9. Teixeira MG, Siqueira JB Jr, Ferreira GL, Africa (2). Twenty-one cases of Lyme Eyal Meltzer,1 Yaniv Lustig,1 Bricks L, Joint G. Epidemiological trends disease were reported in Algiers, Al- Ora Glichinsky, Florian Steiner, of dengue disease in Brazil (2000–2010): a systematic literature search and analysis. geria, during 1996–1999 (3). How- and Eli Schwartz PLoS Negl Trop Dis. 2013;7:e2520. http:// ever, these cases were diagnosed by Author affiliations: The Chaim Sheba Medi- dx.doi.org/10.1371/journal.pntd.0002520 detection of only serum antibodies cal Center Department of Medicine ‘C’ 10. Parreira R, Centeno-Lima S, Lopes A, Portugal-Calisto D, Constantino A, against B. burgdorferi by ELISA with- and Center for Geographic Medicine, Tel Nina J. Dengue virus serotype 4 and chi- out confirmation by Western blotting. Hashomer, Israel (E. Meltzer, E. Schwartz); kungunya virus coinfection in a traveller I. ricinus ticks are also known Tel Aviv University Sackler School of returning from Luanda, Angola, January to harbor spotted fever group rickett- Medicine, Tel Aviv, Israel (E. Meltzer, E. 2014. Euro Surveill. 2014;19:pii:20730. siae, including Rickettsia monacensis, Schwartz); Ministry of Health Central which was detected in Algeria in 2009 Virology Laboratory, Tel Hashomer Address for correspondence: Eli Schwartz, (4). This rickettsia has been recently (Y. Lustig, O. Glichinsky; and Institute of The Center for Geographic Medicine and identified as a human pathogen in Tropical Medicine and International Health, Department of Medicine C, The Chaim Sheba Spain and Italy (5). Charité-Universitätsmedizin Berlin, Berlin, Medical Center, Tel Hashomer, 52621 Israel; To investigate Lyme disease and Germany (F. Steiner) email: [email protected] tickborne rickettsioses transmitted by DOI: http://dx.doi.org/10.3201/eid2010.140609 Table of Contents I. ricinus ticks in northeastern Alge- Emailed to you ria, we collected ticks by using the flag References method in El Ghora (Bougous, El Tarf) (36°39′34″N, 8°22′10″E). Ectopara- 1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, sites were collected in March 2012 and et al. The global distribution and burden of identified to genus and species by using dengue. Nature. 2013;496:504–7. http:// taxonomic morphologic keys (6). dx.doi.org/10.1038/nature12060 Total genomic DNA was isolated 2. Were F. The dengue situation in Africa. Paediatr Int Child Health. 2012;32 Suppl by using the QIAamp Tissue Kit (QIA- 1:18–21. http://dx.doi.org/10.1179/20469 GEN, Hilden, Germany) and BioRobot 04712Z.00000000048 EZ1 (QIAGEN) as described by the 3. Schwartz E, Meltzer E, Mendelson M, manufacturer. DNA was used as tem- Tooke A, Steiner F, Gautret P, et al. Detection on four continents of dengue plate for quantitative real-time PCR. fever cases related to an ongoing outbreak We used the RKND03 system, which is in Luanda, Angola, March to May 2013. specific for the gltA gene of Rickettsia Euro Surveill. 2013;18:pii:20488. spp. (7), and the Bor16S system, which 4. Ongoing dengue epidemic—Angola, June 2013. MMWR Morb Mortal Wkly Rep. GovDelivery is specific for the rrs gene of Borrelia 2013;62:504–7.
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