Skip to main content
Top
Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Co-circulation and simultaneous co-infection of dengue, chikungunya, and zika viruses in patients with febrile syndrome at the Colombian-Venezuelan border

Authors: Marlen Yelitza Carrillo-Hernández, Julian Ruiz-Saenz, Lucy Jaimes Villamizar, Sergio Yebrail Gómez-Rangel, Marlen Martínez-Gutierrez

Published in: BMC Infectious Diseases | Issue 1/2018

Login to get access

Abstract

Background

In Colombia, the dengue virus (DENV) has been endemic for decades, and with the recent entry of the chikungunya virus (CHIKV) (2014) and the Zika virus (ZIKV) (2015), health systems are overloaded because the diagnosis of these three diseases is based on clinical symptoms, and the three diseases share a symptomatology of febrile syndrome. Thus, the objective of this study was to use molecular methods to identify their co-circulation as well as the prevalence of co-infections, in a cohort of patients at the Colombian-Venezuelan border.

Methods

A total of 157 serum samples from patients with febrile syndrome consistent with DENV were collected after informed consent and processed for the identification of DENV (conventional PCR and real-time PCR), CHIKV (conventional PCR), and ZIKV (real-time PCR). DENV-positive samples were serotyped, and some of those positive for DENV and CHIKV were sequenced.

Results

Eighty-two patients were positive for one or more viruses: 33 (21.02%) for DENV, 47 (29.94%) for CHIKV, and 29 (18.47%) for ZIKV. The mean age range of the infected population was statistically higher in the patients infected with ZIKV (29.72 years) than in those infected with DENV or CHIKV (21.09 years). Both co-circulation and co-infection of these three viruses was found. The prevalence of DENV/CHIKV, DENV/ZIKV, and CHIKV/ZIKV co-infection was 7.64%, 6.37%, and 5.10%, with attack rates of 14.90, 12.42, and 9.93 cases per 100,000 inhabitants, respectively. Furthermore, three patients were found to be co-infected with all three viruses (prevalence of 1.91%), with an attack rate of 4.96 cases per 100,000 inhabitants.

Conclusion

Our results demonstrate the simultaneous co-circulation of DENV, CHIKV, ZIKV and their co-infections at the Colombian-Venezuelan border. Moreover, it is necessary to improve the differential diagnosis in patients with acute febrile syndrome and to study the possible consequences of this epidemiological overview of the clinical outcomes of these diseases in endemic regions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Wilder-Smith A, Byass P. The elusive global burden of dengue. Lancet Infect Dis. 2016;16(6):629–31.CrossRefPubMed Wilder-Smith A, Byass P. The elusive global burden of dengue. Lancet Infect Dis. 2016;16(6):629–31.CrossRefPubMed
2.
go back to reference Organization WH, Research SPF, Diseases TiT, diseases WHODoCoNT, Epidemic WHO, Alert P: Dengue: guidelines for diagnosis, treatment, prevention and control: World health Organization; 2009. Organization WH, Research SPF, Diseases TiT, diseases WHODoCoNT, Epidemic WHO, Alert P: Dengue: guidelines for diagnosis, treatment, prevention and control: World health Organization; 2009.
4.
5.
go back to reference Musso D, Cao-Lormeau VM, Gubler DJ. Zika virus: following the path of dengue and chikungunya? Lancet. 2015;386(9990):243–4.CrossRefPubMed Musso D, Cao-Lormeau VM, Gubler DJ. Zika virus: following the path of dengue and chikungunya? Lancet. 2015;386(9990):243–4.CrossRefPubMed
6.
go back to reference Rodenhuis-Zybert IA, Wilschut J, Smit JM. Dengue virus life cycle: viral and host factors modulating infectivity. Cell Mol Life Sci. 2010;67(16):2773–86.CrossRefPubMed Rodenhuis-Zybert IA, Wilschut J, Smit JM. Dengue virus life cycle: viral and host factors modulating infectivity. Cell Mol Life Sci. 2010;67(16):2773–86.CrossRefPubMed
7.
go back to reference Gutierrez G, Gresh L, Perez MA, Elizondo D, Aviles W, Kuan G, Balmaseda A, Harris E. Evaluation of the diagnostic utility of the traditional and revised WHO dengue case definitions. PLoS Negl Trop Dis. 2013;7(8):e2385.CrossRefPubMedPubMedCentral Gutierrez G, Gresh L, Perez MA, Elizondo D, Aviles W, Kuan G, Balmaseda A, Harris E. Evaluation of the diagnostic utility of the traditional and revised WHO dengue case definitions. PLoS Negl Trop Dis. 2013;7(8):e2385.CrossRefPubMedPubMedCentral
9.
go back to reference Omarjee R, Prat C, Flusin O, Boucau S, Tenebray B, Merle O, Huc-Anais P, Cassadou S, Leparc-Goffart I. Importance of case definition to monitor ongoing outbreak of chikungunya virus on a background of actively circulating dengue virus, St Martin, December 2013 to January 2014. Euro Surveill. 2014;19(13):20753.CrossRefPubMed Omarjee R, Prat C, Flusin O, Boucau S, Tenebray B, Merle O, Huc-Anais P, Cassadou S, Leparc-Goffart I. Importance of case definition to monitor ongoing outbreak of chikungunya virus on a background of actively circulating dengue virus, St Martin, December 2013 to January 2014. Euro Surveill. 2014;19(13):20753.CrossRefPubMed
10.
go back to reference Furuya-Kanamori L, Liang S, Milinovich G, RJS M, ACA C, Hu W, Brasil P, Frentiu FD, Dunning R, Yakob L. Co-distribution and co-infection of chikungunya and dengue viruses. BMC Infect Dis. 2016;16(84):1. Furuya-Kanamori L, Liang S, Milinovich G, RJS M, ACA C, Hu W, Brasil P, Frentiu FD, Dunning R, Yakob L. Co-distribution and co-infection of chikungunya and dengue viruses. BMC Infect Dis. 2016;16(84):1.
11.
go back to reference Soumahoro MK, Gerardin P, Boelle PY, Perrau J, Fianu A, Pouchot J, Malvy D, Flahault A, Favier F, Hanslik T. Impact of chikungunya virus infection on health status and quality of life: a retrospective cohort study. PLoS One. 2009;4(11):e7800.CrossRefPubMedPubMedCentral Soumahoro MK, Gerardin P, Boelle PY, Perrau J, Fianu A, Pouchot J, Malvy D, Flahault A, Favier F, Hanslik T. Impact of chikungunya virus infection on health status and quality of life: a retrospective cohort study. PLoS One. 2009;4(11):e7800.CrossRefPubMedPubMedCentral
12.
go back to reference Rodríguez-morales AJ, Cardona-ospina JA, Urbano-Garzón SF, Hurtado-Zapata JS. Prevalence of post-chikungunya chronic inflammatory rheumatism: a systematic review and meta-analysis. Arthritis Care Res (Hoboken). 2016;68(12):1849–58.CrossRef Rodríguez-morales AJ, Cardona-ospina JA, Urbano-Garzón SF, Hurtado-Zapata JS. Prevalence of post-chikungunya chronic inflammatory rheumatism: a systematic review and meta-analysis. Arthritis Care Res (Hoboken). 2016;68(12):1849–58.CrossRef
13.
go back to reference Cao-Lormeau VM, Blake A, Mons S, Lastere S, Roche C, Vanhomwegen J, Dub T, Baudouin L, Teissier A, Larre P, et al. Guillain-Barre syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet. 2016;387(10027):1531–9.CrossRefPubMedPubMedCentral Cao-Lormeau VM, Blake A, Mons S, Lastere S, Roche C, Vanhomwegen J, Dub T, Baudouin L, Teissier A, Larre P, et al. Guillain-Barre syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet. 2016;387(10027):1531–9.CrossRefPubMedPubMedCentral
14.
go back to reference Estofolete CF, Terzian ACB, Parreira R, Esteves A, Hardman L, Greque GV, Rahal P, Nogueira ML. Clinical and laboratory profile of Zika virus infection in dengue suspected patients: a case series. J Clin Virol. 2016;81:25–30.CrossRef Estofolete CF, Terzian ACB, Parreira R, Esteves A, Hardman L, Greque GV, Rahal P, Nogueira ML. Clinical and laboratory profile of Zika virus infection in dengue suspected patients: a case series. J Clin Virol. 2016;81:25–30.CrossRef
15.
go back to reference Acevedo N, Waggoner J, Rodriguez M, Rivera L, Landivar J, Pinsky B, Zambrano H. Zika virus, chikungunya virus, and dengue virus in cerebrospinal fluid from adults with neurological manifestations, Guayaquil, Ecuador. Front Microbiol. 2017;8:42.CrossRefPubMedPubMedCentral Acevedo N, Waggoner J, Rodriguez M, Rivera L, Landivar J, Pinsky B, Zambrano H. Zika virus, chikungunya virus, and dengue virus in cerebrospinal fluid from adults with neurological manifestations, Guayaquil, Ecuador. Front Microbiol. 2017;8:42.CrossRefPubMedPubMedCentral
16.
go back to reference Villar LA, Rojas DP, Besada-Lombana S, Sarti E. Epidemiological trends of dengue disease in Colombia (2000-2011): a systematic review. PLoS Negl Trop Dis. 2015;9(3):e0003499.CrossRefPubMedPubMedCentral Villar LA, Rojas DP, Besada-Lombana S, Sarti E. Epidemiological trends of dengue disease in Colombia (2000-2011): a systematic review. PLoS Negl Trop Dis. 2015;9(3):e0003499.CrossRefPubMedPubMedCentral
17.
go back to reference Martinez-Gutierrez M, Ruiz-Saenz J. Chikungunya in Colombia: chronicle of an epidemic foretold. Curare. 2014;1(2):39–41. Martinez-Gutierrez M, Ruiz-Saenz J. Chikungunya in Colombia: chronicle of an epidemic foretold. Curare. 2014;1(2):39–41.
18.
go back to reference Mattar S, Miranda J, Pinzon H, Tique V, Bolanos A, Aponte J, Arrieta G, Gonzalez M, Barrios K, Contreras H, et al. Outbreak of chikungunya virus in the north Caribbean area of Colombia: clinical presentation and phylogenetic analysis. J Infect Dev Ctries. 2015;9(10):1126–32.CrossRefPubMed Mattar S, Miranda J, Pinzon H, Tique V, Bolanos A, Aponte J, Arrieta G, Gonzalez M, Barrios K, Contreras H, et al. Outbreak of chikungunya virus in the north Caribbean area of Colombia: clinical presentation and phylogenetic analysis. J Infect Dev Ctries. 2015;9(10):1126–32.CrossRefPubMed
19.
go back to reference Pacheco O, Beltran M, Nelson CA, Valencia D, Tolosa N, Farr SL, Padilla AV, Tong VT, Cuevas EL, Espinosa-Bode A, et al. Zika virus disease in Colombia - preliminary report. N Engl J Med. 2016; Pacheco O, Beltran M, Nelson CA, Valencia D, Tolosa N, Farr SL, Padilla AV, Tong VT, Cuevas EL, Espinosa-Bode A, et al. Zika virus disease in Colombia - preliminary report. N Engl J Med. 2016;
20.
go back to reference Alarcon-Cruz AP, Prieto-Suarez E. Description of the process of preparation and response of local health authorities facing the introduction of the chikungunya virus in Colombia, 2014. Rev Salud Publica (Bogota). 2016;18(3):331–43.CrossRef Alarcon-Cruz AP, Prieto-Suarez E. Description of the process of preparation and response of local health authorities facing the introduction of the chikungunya virus in Colombia, 2014. Rev Salud Publica (Bogota). 2016;18(3):331–43.CrossRef
23.
go back to reference Villamil-Gomez WE, Gonzalez-Camargo O, Rodriguez-Ayubi J, Zapata-Serpa D, Rodriguez-Morales AJ. Dengue, chikungunya and Zika co-infection in a patient from Colombia. J Infect Public Health. 2016;9(5):684–6.CrossRefPubMed Villamil-Gomez WE, Gonzalez-Camargo O, Rodriguez-Ayubi J, Zapata-Serpa D, Rodriguez-Morales AJ. Dengue, chikungunya and Zika co-infection in a patient from Colombia. J Infect Public Health. 2016;9(5):684–6.CrossRefPubMed
24.
go back to reference Sardi SI, Somasekar S, Naccache SN, Bandeira AC, Tauro LB, Campos GS, Chiu CY. Co-infections from Zika and chikungunya virus in Bahia, Brazil identified by metagenomic next-generation sequencing. J Clin Microbiol. 2016;54(9):2348–53.CrossRefPubMedPubMedCentral Sardi SI, Somasekar S, Naccache SN, Bandeira AC, Tauro LB, Campos GS, Chiu CY. Co-infections from Zika and chikungunya virus in Bahia, Brazil identified by metagenomic next-generation sequencing. J Clin Microbiol. 2016;54(9):2348–53.CrossRefPubMedPubMedCentral
25.
go back to reference Villamil-Gomez WE, Rodriguez-Morales AJ, Uribe-Garcia AM, Gonzalez-Arismendy E, Castellanos JE, Calvo EP, Alvarez-Mon M, Musso D. Zika, dengue, and chikungunya co-infection in a pregnant woman from Colombia. Int J Infect Dis. 2016;51:135–8.CrossRefPubMed Villamil-Gomez WE, Rodriguez-Morales AJ, Uribe-Garcia AM, Gonzalez-Arismendy E, Castellanos JE, Calvo EP, Alvarez-Mon M, Musso D. Zika, dengue, and chikungunya co-infection in a pregnant woman from Colombia. Int J Infect Dis. 2016;51:135–8.CrossRefPubMed
26.
go back to reference Pessôa R, Patriota JV, Md L d S, Felix AC, Mamede N, Sanabani SS. Investigation into an outbreak of dengue-like illness in Pernambuco, Brazil, revealed a Cocirculation of Zika, chikungunya, and dengue virus type 1. Medicine (Baltimore). 2016;95(12):e3201.CrossRef Pessôa R, Patriota JV, Md L d S, Felix AC, Mamede N, Sanabani SS. Investigation into an outbreak of dengue-like illness in Pernambuco, Brazil, revealed a Cocirculation of Zika, chikungunya, and dengue virus type 1. Medicine (Baltimore). 2016;95(12):e3201.CrossRef
27.
go back to reference Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses. J Clin Microbiol. 2006;44(4):1295–304.CrossRefPubMedPubMedCentral Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses. J Clin Microbiol. 2006;44(4):1295–304.CrossRefPubMedPubMedCentral
28.
go back to reference Waggoner JJ, Abeynayake J, Sahoo MK, Gresh L, Tellez Y, Gonzalez K, Ballesteros G, Pierro AM, Gaibani P, Guo FP, et al. Single-reaction, multiplex, real-time rt-PCR for the detection, quantitation, and serotyping of dengue viruses. PLoS Negl Trop Dis. 2013;7(4):e2116.CrossRefPubMedPubMedCentral Waggoner JJ, Abeynayake J, Sahoo MK, Gresh L, Tellez Y, Gonzalez K, Ballesteros G, Pierro AM, Gaibani P, Guo FP, et al. Single-reaction, multiplex, real-time rt-PCR for the detection, quantitation, and serotyping of dengue viruses. PLoS Negl Trop Dis. 2013;7(4):e2116.CrossRefPubMedPubMedCentral
29.
go back to reference Pfeffer M, Linssen B, Parker MD, Kinney RM. Specific detection of chikungunya virus using a RT-PCR/nested PCR combination. J Vet Med B Infect Dis Vet Public Health. 2002;49(1):49–54.CrossRefPubMed Pfeffer M, Linssen B, Parker MD, Kinney RM. Specific detection of chikungunya virus using a RT-PCR/nested PCR combination. J Vet Med B Infect Dis Vet Public Health. 2002;49(1):49–54.CrossRefPubMed
30.
go back to reference Gomez-Calderon C, Mesa-Castro C, Robledo S, Gomez S, Bolivar-Avila S, Diaz-Castillo F, Martinez-Gutierrez M. Antiviral effect of compounds derived from the seeds of Mammea Americana and Tabernaemontana Cymosa on dengue and chikungunya virus infections. BMC Complement Altern Med. 2017;17(1):57.CrossRefPubMedPubMedCentral Gomez-Calderon C, Mesa-Castro C, Robledo S, Gomez S, Bolivar-Avila S, Diaz-Castillo F, Martinez-Gutierrez M. Antiviral effect of compounds derived from the seeds of Mammea Americana and Tabernaemontana Cymosa on dengue and chikungunya virus infections. BMC Complement Altern Med. 2017;17(1):57.CrossRefPubMedPubMedCentral
31.
go back to reference Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR. Genetic and serologic properties of Zika virus associated with an epidemic, yap state, Micronesia, 2007. Emerg Infect Dis. 2008;14(8):1232–9.CrossRefPubMedPubMedCentral Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR. Genetic and serologic properties of Zika virus associated with an epidemic, yap state, Micronesia, 2007. Emerg Infect Dis. 2008;14(8):1232–9.CrossRefPubMedPubMedCentral
33.
go back to reference L'Huillier AG, Lombos E, Tang E, Perusini S, Eshaghi A, Nagra S, Frantz C, Olsha R, Kristjanson E, Dimitrova K, et al. Evaluation of Altona diagnostics RealStar Zika virus reverse transcription-PCR test kit for Zika virus PCR testing. J Clin Microbiol. 2017;55(5):1576–84.CrossRefPubMedPubMedCentral L'Huillier AG, Lombos E, Tang E, Perusini S, Eshaghi A, Nagra S, Frantz C, Olsha R, Kristjanson E, Dimitrova K, et al. Evaluation of Altona diagnostics RealStar Zika virus reverse transcription-PCR test kit for Zika virus PCR testing. J Clin Microbiol. 2017;55(5):1576–84.CrossRefPubMedPubMedCentral
34.
go back to reference Paiva MHS, Guedes DRD, Leal WS, Ayres CFJ. Sensitivity of RT-PCR method in samples shown to be positive for Zika virus by RT-qPCR in vector competence studies. Genet Mol Biol. 2017;40(3):597–9.CrossRefPubMedPubMedCentral Paiva MHS, Guedes DRD, Leal WS, Ayres CFJ. Sensitivity of RT-PCR method in samples shown to be positive for Zika virus by RT-qPCR in vector competence studies. Genet Mol Biol. 2017;40(3):597–9.CrossRefPubMedPubMedCentral
35.
go back to reference Faye O, Faye O, Diallo D, Diallo M, Weidmann M, Sall AA. Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes. Virol J. 2013;10(1):311.CrossRefPubMedPubMedCentral Faye O, Faye O, Diallo D, Diallo M, Weidmann M, Sall AA. Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes. Virol J. 2013;10(1):311.CrossRefPubMedPubMedCentral
36.
go back to reference Naccache S, Theze J, Sardi SI, Somasekar S, Greninger AL, Bandeira AC, Campos GS, Tauro LB, Faria NR, Pybus OG. Distinct Zika virus lineage in Salvador, Bahia, Brazil. Emerg Infect Dis. 2016;22(10):1788–92.CrossRefPubMedPubMedCentral Naccache S, Theze J, Sardi SI, Somasekar S, Greninger AL, Bandeira AC, Campos GS, Tauro LB, Faria NR, Pybus OG. Distinct Zika virus lineage in Salvador, Bahia, Brazil. Emerg Infect Dis. 2016;22(10):1788–92.CrossRefPubMedPubMedCentral
37.
go back to reference Diaz-Quijano F, Gonzalez-Rangel A, Gomez-Capacho A, Espindola-Gomez R, Martinez-Vega R, Villar-Centeno L. Rrainfall and acute febrile syndrome in a dengue-endemic area. Rev Salud Publica (Bogota). 2008;10(2):250–9.CrossRef Diaz-Quijano F, Gonzalez-Rangel A, Gomez-Capacho A, Espindola-Gomez R, Martinez-Vega R, Villar-Centeno L. Rrainfall and acute febrile syndrome in a dengue-endemic area. Rev Salud Publica (Bogota). 2008;10(2):250–9.CrossRef
38.
go back to reference Rodríguez-Villamarín FR, Prieto-Suarez E, Escandón PL, de la Hoz Restrepo F. Leptospirosis percentage and related factors in patients having a presumptive diagnosis of dengue, 2010-2012. Rev Salud Publica (Bogota). 2014;16(4):597–609.CrossRef Rodríguez-Villamarín FR, Prieto-Suarez E, Escandón PL, de la Hoz Restrepo F. Leptospirosis percentage and related factors in patients having a presumptive diagnosis of dengue, 2010-2012. Rev Salud Publica (Bogota). 2014;16(4):597–609.CrossRef
39.
go back to reference Gomez Arcila V, Arroyo Salgado BJ, Bello Espinosa AA, Rodriguez Escobar Z, Polo Andrade ER. Microbiological diagnosis compatible with Anaplasma sp. in a patient suffering from febrile syndrome. Rev Argent Microbiol. 2015;47(1):78–9.PubMed Gomez Arcila V, Arroyo Salgado BJ, Bello Espinosa AA, Rodriguez Escobar Z, Polo Andrade ER. Microbiological diagnosis compatible with Anaplasma sp. in a patient suffering from febrile syndrome. Rev Argent Microbiol. 2015;47(1):78–9.PubMed
40.
go back to reference Mattar S, Garzon D, Tadeu L, Faccini-Martinez AA, Mills JN. Serological diagnosis of hantavirus pulmonary syndrome in a febrile patient in Colombia. Int J Infect Dis. 2014;25:201–3.CrossRefPubMed Mattar S, Garzon D, Tadeu L, Faccini-Martinez AA, Mills JN. Serological diagnosis of hantavirus pulmonary syndrome in a febrile patient in Colombia. Int J Infect Dis. 2014;25:201–3.CrossRefPubMed
41.
go back to reference Arroyave E, Londono AF, Quintero JC, Agudelo-Florez P, Arboleda M, Diaz FJ, Rodas JD. Etiology and epidemiological characterization of non-malarial febrile syndrome in three municipalities of Uraba (Antioquia), Colombia. Biomedica. 2013;33(Suppl 1):99–107.PubMed Arroyave E, Londono AF, Quintero JC, Agudelo-Florez P, Arboleda M, Diaz FJ, Rodas JD. Etiology and epidemiological characterization of non-malarial febrile syndrome in three municipalities of Uraba (Antioquia), Colombia. Biomedica. 2013;33(Suppl 1):99–107.PubMed
42.
go back to reference Romero-Vega L, Pacheco O, de la Hoz-Restrepo F, Diaz-Quijano FA. Evaluation of dengue fever reports during an epidemic, Colombia. Rev Saude Publica. 2014;48(6):899–905.CrossRefPubMedPubMedCentral Romero-Vega L, Pacheco O, de la Hoz-Restrepo F, Diaz-Quijano FA. Evaluation of dengue fever reports during an epidemic, Colombia. Rev Saude Publica. 2014;48(6):899–905.CrossRefPubMedPubMedCentral
43.
go back to reference Ocazionez RE, Gómez SY, Cortés FM. Dengue hemorrhagic fever serotype and infection pattern in a Colombian endemic area. Rev Salud Publica (Bogota). 2007;9(2):262–74.CrossRef Ocazionez RE, Gómez SY, Cortés FM. Dengue hemorrhagic fever serotype and infection pattern in a Colombian endemic area. Rev Salud Publica (Bogota). 2007;9(2):262–74.CrossRef
44.
go back to reference Alvis-Guzman N, Rodriguez-Barreto H, Mattar-Velilla S. Dengue in an area of the Colombian Caribbean. Colomb Med (Cali). 2015;46(1):3–7. Alvis-Guzman N, Rodriguez-Barreto H, Mattar-Velilla S. Dengue in an area of the Colombian Caribbean. Colomb Med (Cali). 2015;46(1):3–7.
45.
go back to reference Ramachandran VG, Das S, Roy P, Hada V, Mogha NS. Chikungunya: a reemerging infection spreading during 2010 dengue fever outbreak in National Capital Region of India. Virusdisease. 2016;27(2):183–6.CrossRefPubMedPubMedCentral Ramachandran VG, Das S, Roy P, Hada V, Mogha NS. Chikungunya: a reemerging infection spreading during 2010 dengue fever outbreak in National Capital Region of India. Virusdisease. 2016;27(2):183–6.CrossRefPubMedPubMedCentral
46.
go back to reference Singh P, Mittal V, Rizvi MMA, Chhabra M, Sharma P, Rawat DS, Bhattacharya D, Chauhan LS, Rai A. The first dominant co-circulation of both dengue and chikungunya viruses during the post-monsoon period of 2010 in Delhi, India. Epidemiol Infect. 2012;140(7):1337–42.CrossRefPubMed Singh P, Mittal V, Rizvi MMA, Chhabra M, Sharma P, Rawat DS, Bhattacharya D, Chauhan LS, Rai A. The first dominant co-circulation of both dengue and chikungunya viruses during the post-monsoon period of 2010 in Delhi, India. Epidemiol Infect. 2012;140(7):1337–42.CrossRefPubMed
47.
go back to reference Carabali M, Lim JK, Velez DC, Trujillo A, Egurrola J, Lee KS, Kaufman JS, DaSilva LJ, Velez ID, Osorio JE. Dengue virus serological prevalence and seroconversion rates in children and adults in Medellin, Colombia: implications for vaccine introduction. Int J Infect Dis. 2017;58:27–36.CrossRefPubMedPubMedCentral Carabali M, Lim JK, Velez DC, Trujillo A, Egurrola J, Lee KS, Kaufman JS, DaSilva LJ, Velez ID, Osorio JE. Dengue virus serological prevalence and seroconversion rates in children and adults in Medellin, Colombia: implications for vaccine introduction. Int J Infect Dis. 2017;58:27–36.CrossRefPubMedPubMedCentral
48.
go back to reference Roth A, Mercier A, Lepers C, Hoy D, Duituturaga S, Benyon E, Guillaumot L, Souares Y. Concurrent outbreaks of dengue, chikungunya and Zika virus infections - an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012-2014. Euro Surveill. 2014;19(41):20929.CrossRefPubMed Roth A, Mercier A, Lepers C, Hoy D, Duituturaga S, Benyon E, Guillaumot L, Souares Y. Concurrent outbreaks of dengue, chikungunya and Zika virus infections - an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012-2014. Euro Surveill. 2014;19(41):20929.CrossRefPubMed
49.
go back to reference Cardona-Ospina JA, Villamil-Gomez WE, Jimenez-Canizales CE, Castaneda-Hernandez DM, Rodriguez-Morales AJ. Estimating the burden of disease and the economic cost attributable to chikungunya, Colombia, 2014. Trans R Soc Trop Med Hyg. 2015;109(12):793–802.CrossRefPubMed Cardona-Ospina JA, Villamil-Gomez WE, Jimenez-Canizales CE, Castaneda-Hernandez DM, Rodriguez-Morales AJ. Estimating the burden of disease and the economic cost attributable to chikungunya, Colombia, 2014. Trans R Soc Trop Med Hyg. 2015;109(12):793–802.CrossRefPubMed
50.
go back to reference Teixeira MG, Siqueira JB Jr, Ferreira GL, Bricks L, Joint G. Epidemiological trends of dengue disease in Brazil (2000-2010): a systematic literature search and analysis. PLoS Negl Trop Dis. 2013;7(12):e2520.CrossRefPubMedPubMedCentral Teixeira MG, Siqueira JB Jr, Ferreira GL, Bricks L, Joint G. Epidemiological trends of dengue disease in Brazil (2000-2010): a systematic literature search and analysis. PLoS Negl Trop Dis. 2013;7(12):e2520.CrossRefPubMedPubMedCentral
51.
go back to reference San Martin JL, Brathwaite O, Zambrano B, Solorzano JO, Bouckenooghe A, Dayan GH, Guzman MG. The epidemiology of dengue in the americas over the last three decades: a worrisome reality. Am J Trop Med Hyg. 2010;82(1):128–35.CrossRefPubMedPubMedCentral San Martin JL, Brathwaite O, Zambrano B, Solorzano JO, Bouckenooghe A, Dayan GH, Guzman MG. The epidemiology of dengue in the americas over the last three decades: a worrisome reality. Am J Trop Med Hyg. 2010;82(1):128–35.CrossRefPubMedPubMedCentral
52.
go back to reference Berger S: Chikungunya and Zika: Global Status: 2016 Edition. In. Edited by Berger S. Los Angeles, California, USA.: GIDEON Informatics, Inc.; 2016: 121. Berger S: Chikungunya and Zika: Global Status: 2016 Edition. In. Edited by Berger S. Los Angeles, California, USA.: GIDEON Informatics, Inc.; 2016: 121.
53.
go back to reference Dirlikov E. Update: ongoing Zika virus transmission—Puerto Rico, November 1, 2015–April 14, 2016. MMWR Morb Mortal Wkly Rep. 2016;65 Dirlikov E. Update: ongoing Zika virus transmission—Puerto Rico, November 1, 2015–April 14, 2016. MMWR Morb Mortal Wkly Rep. 2016;65
54.
go back to reference Morrison AC, Zielinski-Gutierrez E, Scott TW, Rosenberg R. Defining challenges and proposing solutions for control of the virus vector Aedes Aegypti. PLoS Med. 2008;5(3):e68.CrossRefPubMedPubMedCentral Morrison AC, Zielinski-Gutierrez E, Scott TW, Rosenberg R. Defining challenges and proposing solutions for control of the virus vector Aedes Aegypti. PLoS Med. 2008;5(3):e68.CrossRefPubMedPubMedCentral
55.
go back to reference Mlakar J, Korva M, Tul N, Popovic M, Poljsak-Prijatelj M, Mraz J, Kolenc M, Resman Rus K, Vesnaver Vipotnik T, Fabjan Vodusek V, et al. Zika virus associated with microcephaly. N Engl J Med. 2016;374(10):951–8.CrossRefPubMed Mlakar J, Korva M, Tul N, Popovic M, Poljsak-Prijatelj M, Mraz J, Kolenc M, Resman Rus K, Vesnaver Vipotnik T, Fabjan Vodusek V, et al. Zika virus associated with microcephaly. N Engl J Med. 2016;374(10):951–8.CrossRefPubMed
56.
go back to reference Valentine G, Marquez L, Pammi M. Zika virus-associated microcephaly and eye lesions in the newborn. J Pediatric Infect Dis Soc. 2016;5(3):323–8.CrossRefPubMed Valentine G, Marquez L, Pammi M. Zika virus-associated microcephaly and eye lesions in the newborn. J Pediatric Infect Dis Soc. 2016;5(3):323–8.CrossRefPubMed
58.
go back to reference Weaver SC, Vasilakis N. Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infect Genet Evol. 2009;9(4):523–40.CrossRefPubMedPubMedCentral Weaver SC, Vasilakis N. Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infect Genet Evol. 2009;9(4):523–40.CrossRefPubMedPubMedCentral
59.
go back to reference Ocazionez-Jiménez RE, Ortiz-Báez AS, Gómez-Rangel SY, Miranda-Esquivel DR. Dengue virus serotype 1 (DENV-1) from Colombia: its contribution to dengue occurrence in Santander. Biomedica. 2013;33(Supl 1):22–30.PubMed Ocazionez-Jiménez RE, Ortiz-Báez AS, Gómez-Rangel SY, Miranda-Esquivel DR. Dengue virus serotype 1 (DENV-1) from Colombia: its contribution to dengue occurrence in Santander. Biomedica. 2013;33(Supl 1):22–30.PubMed
60.
go back to reference Gómez S, Villabona-Arenas C, Torres FA, Miranda-Esquivel D, Ocazionez RE. Dengue virus serotype-3 (genotype III) from Colombia: perspective of its pathogenic potential. Dengue Bulletin. 2008;32:126–37. Gómez S, Villabona-Arenas C, Torres FA, Miranda-Esquivel D, Ocazionez RE. Dengue virus serotype-3 (genotype III) from Colombia: perspective of its pathogenic potential. Dengue Bulletin. 2008;32:126–37.
61.
go back to reference Laiton-Donato K, Usme-Ciro JA, Rico A, Pardo L, Martínez C, Salas D, Ardila S, Páez A. Phylogenetic analysis of chikungunya virus in Colombia: evidence of purifying selection in the E1 gene. Biomedica. 2015;36(0):25–34.CrossRefPubMed Laiton-Donato K, Usme-Ciro JA, Rico A, Pardo L, Martínez C, Salas D, Ardila S, Páez A. Phylogenetic analysis of chikungunya virus in Colombia: evidence of purifying selection in the E1 gene. Biomedica. 2015;36(0):25–34.CrossRefPubMed
62.
go back to reference Rodas JD, Kautz T, Camacho E, Paternina L, Guzman H, Diaz FJ, Blanco P, Tesh R, Weaver SC. Genetic characterization of northwestern Colombian chikungunya virus strains from the 2014-2015 epidemic. Am J Trop Med Hyg. 2016;95(3):639–46.CrossRefPubMedPubMedCentral Rodas JD, Kautz T, Camacho E, Paternina L, Guzman H, Diaz FJ, Blanco P, Tesh R, Weaver SC. Genetic characterization of northwestern Colombian chikungunya virus strains from the 2014-2015 epidemic. Am J Trop Med Hyg. 2016;95(3):639–46.CrossRefPubMedPubMedCentral
63.
go back to reference Diaz-Quinonez JA, Escobar-Escamilla N, Wong-Arambula C, Vazquez-Pichardo M, Torres-Longoria B, Lopez-Martinez I, Ruiz-Matus C, Kuri-Morales P, Ramirez-Gonzalez JE. Asian genotype Zika virus detected in traveler returning to Mexico from Colombia, October 2015. Emerg Infect Dis. 2016;22(5):937–9.CrossRefPubMedPubMedCentral Diaz-Quinonez JA, Escobar-Escamilla N, Wong-Arambula C, Vazquez-Pichardo M, Torres-Longoria B, Lopez-Martinez I, Ruiz-Matus C, Kuri-Morales P, Ramirez-Gonzalez JE. Asian genotype Zika virus detected in traveler returning to Mexico from Colombia, October 2015. Emerg Infect Dis. 2016;22(5):937–9.CrossRefPubMedPubMedCentral
64.
65.
go back to reference Saswat T, Kumar A, Kumar S, Mamidi P, Muduli S, Debata NK, Pal NS, Pratheek BM, Chattopadhyay S, Chattopadhyay S. High rates of co-infection of dengue and chikungunya virus in Odisha and Maharashtra, India during 2013. Infect Genet Evol. 2015;35:134–41.CrossRefPubMed Saswat T, Kumar A, Kumar S, Mamidi P, Muduli S, Debata NK, Pal NS, Pratheek BM, Chattopadhyay S, Chattopadhyay S. High rates of co-infection of dengue and chikungunya virus in Odisha and Maharashtra, India during 2013. Infect Genet Evol. 2015;35:134–41.CrossRefPubMed
67.
go back to reference Drumond BP, Mondini A, Schmidt DJ, de Morais Bronzoni RV, Bosch I, Nogueira ML. Circulation of different lineages of dengue virus 2, genotype American/Asian in Brazil: dynamics and molecular and phylogenetic characterization. PLoS One. 2013;8(3):e59422.CrossRefPubMedPubMedCentral Drumond BP, Mondini A, Schmidt DJ, de Morais Bronzoni RV, Bosch I, Nogueira ML. Circulation of different lineages of dengue virus 2, genotype American/Asian in Brazil: dynamics and molecular and phylogenetic characterization. PLoS One. 2013;8(3):e59422.CrossRefPubMedPubMedCentral
68.
go back to reference Yamanaka A, Mulyatno KC, Susilowati H, Hendrianto E, Ginting AP, Sary DD, Rantam FA, Soegijanto S, Konishi E. Displacement of the predominant dengue virus from type 2 to type 1 with a subsequent genotype shift from IV to I in Surabaya, Indonesia 2008-2010. PLoS One. 2011;6(11):e27322.CrossRefPubMedPubMedCentral Yamanaka A, Mulyatno KC, Susilowati H, Hendrianto E, Ginting AP, Sary DD, Rantam FA, Soegijanto S, Konishi E. Displacement of the predominant dengue virus from type 2 to type 1 with a subsequent genotype shift from IV to I in Surabaya, Indonesia 2008-2010. PLoS One. 2011;6(11):e27322.CrossRefPubMedPubMedCentral
69.
go back to reference Chahar HS, Bharaj P, Dar L, Guleria R, Kabra SK, Broor S. Co-infections with chikungunya virus and dengue virus in Delhi, India. Emerg Infect Dis. 2009;15(7):1077–80.CrossRefPubMedPubMedCentral Chahar HS, Bharaj P, Dar L, Guleria R, Kabra SK, Broor S. Co-infections with chikungunya virus and dengue virus in Delhi, India. Emerg Infect Dis. 2009;15(7):1077–80.CrossRefPubMedPubMedCentral
70.
go back to reference Waggoner JJ, Gresh L, Vargas MJ, Ballesteros G, Tellez Y, Soda KJ, Sahoo MK, Nunez A, Balmaseda A, Harris E, et al. Viremia and clinical presentation in Nicaraguan patients infected with Zika virus, chikungunya virus, and dengue virus. Clin Infect Dis. 2016;63(12):1584–90.CrossRefPubMedPubMedCentral Waggoner JJ, Gresh L, Vargas MJ, Ballesteros G, Tellez Y, Soda KJ, Sahoo MK, Nunez A, Balmaseda A, Harris E, et al. Viremia and clinical presentation in Nicaraguan patients infected with Zika virus, chikungunya virus, and dengue virus. Clin Infect Dis. 2016;63(12):1584–90.CrossRefPubMedPubMedCentral
72.
go back to reference Soares CN, Cabral-Castro M, Oliveira C, Faria LC, Peralta JM, Freitas MR, Puccioni-Sohler M. Oligosymptomatic dengue infection: a potential cause of Guillain Barre syndrome. Arq Neuropsiquiatr. 2008;66(2A):234–7.CrossRefPubMed Soares CN, Cabral-Castro M, Oliveira C, Faria LC, Peralta JM, Freitas MR, Puccioni-Sohler M. Oligosymptomatic dengue infection: a potential cause of Guillain Barre syndrome. Arq Neuropsiquiatr. 2008;66(2A):234–7.CrossRefPubMed
73.
go back to reference Villamil-Gomez W, Silvera LA, Paez-Castellanos J, Rodriguez-Morales AJ. Guillain-Barre syndrome after chikungunya infection: a case in Colombia. Enferm Infecc Microbiol Clin. 2016;34(2):140–1.CrossRefPubMed Villamil-Gomez W, Silvera LA, Paez-Castellanos J, Rodriguez-Morales AJ. Guillain-Barre syndrome after chikungunya infection: a case in Colombia. Enferm Infecc Microbiol Clin. 2016;34(2):140–1.CrossRefPubMed
74.
go back to reference Arias A, Torres-Tobar L, Hernandez G, Paipilla D, Palacios E, Torres Y, Duran J, Ugarte US, Ardila-sierra A, Castellanos G. Guillain-Barre syndrome in patients with a recent history of Zika in Cucuta, Colombia: a descriptive case series of 19 patients from December 2015 to march 2016. J Crit Care. 2017;37:19–23.CrossRefPubMed Arias A, Torres-Tobar L, Hernandez G, Paipilla D, Palacios E, Torres Y, Duran J, Ugarte US, Ardila-sierra A, Castellanos G. Guillain-Barre syndrome in patients with a recent history of Zika in Cucuta, Colombia: a descriptive case series of 19 patients from December 2015 to march 2016. J Crit Care. 2017;37:19–23.CrossRefPubMed
75.
go back to reference Mercado M, Acosta-Reyes J, Parra E, Pardo L, Rico A, Campo A, Navarro E, Viasus D. Clinical and histopathological features of fatal cases with dengue and chikungunya virus co-infection in Colombia, 2014 to 2015. Euro Surveill. 2016;21(22) Mercado M, Acosta-Reyes J, Parra E, Pardo L, Rico A, Campo A, Navarro E, Viasus D. Clinical and histopathological features of fatal cases with dengue and chikungunya virus co-infection in Colombia, 2014 to 2015. Euro Surveill. 2016;21(22)
76.
go back to reference Priyamvada L, Quicke KM, Hudson WH, Onlamoon N, Sewatanon J, Edupuganti S, Pattanapanyasat K, Chokephaibulkit K, Mulligan MJ, Wilson PC, et al. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc Natl Acad Sci U S A. 2016;113(28):7852–7.CrossRefPubMedPubMedCentral Priyamvada L, Quicke KM, Hudson WH, Onlamoon N, Sewatanon J, Edupuganti S, Pattanapanyasat K, Chokephaibulkit K, Mulligan MJ, Wilson PC, et al. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc Natl Acad Sci U S A. 2016;113(28):7852–7.CrossRefPubMedPubMedCentral
77.
go back to reference Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G, Duangchinda T, Sakuntabhai A, Cao-Lormeau VM, Malasit P, Rey FA, et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat Immunol. 2016;17(9):1102–8.CrossRefPubMedPubMedCentral Dejnirattisai W, Supasa P, Wongwiwat W, Rouvinski A, Barba-Spaeth G, Duangchinda T, Sakuntabhai A, Cao-Lormeau VM, Malasit P, Rey FA, et al. Dengue virus sero-cross-reactivity drives antibody-dependent enhancement of infection with zika virus. Nat Immunol. 2016;17(9):1102–8.CrossRefPubMedPubMedCentral
78.
go back to reference Kawiecki AB, Christofferson RC. Zika virus-induced antibody response enhances dengue virus serotype 2 replication in vitro. J Infect Dis. 2016;214(9):1357–60.CrossRefPubMed Kawiecki AB, Christofferson RC. Zika virus-induced antibody response enhances dengue virus serotype 2 replication in vitro. J Infect Dis. 2016;214(9):1357–60.CrossRefPubMed
Metadata
Title
Co-circulation and simultaneous co-infection of dengue, chikungunya, and zika viruses in patients with febrile syndrome at the Colombian-Venezuelan border
Authors
Marlen Yelitza Carrillo-Hernández
Julian Ruiz-Saenz
Lucy Jaimes Villamizar
Sergio Yebrail Gómez-Rangel
Marlen Martínez-Gutierrez
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-2976-1

Other articles of this Issue 1/2018

BMC Infectious Diseases 1/2018 Go to the issue