Surveillance for Flaviviruses Near the Mexico–U.S. Border: Co-circulation of Dengue Virus Serotypes 1, 2, and 3 and West Nile Virus in Tamaulipas, Northern Mexico, 2014–2016

S. Viridiana Laredo-Tiscareño Laboratorio de Biomedicina Molecular, Centro de Biotecnología Genómica del Instituto Politécnico Nacional, Reynosa, Tamaulipas, México;
Laboratorio de Arbovirología, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autónoma de Yucatán, Mérida, México;
Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa;

Search for other papers by S. Viridiana Laredo-Tiscareño in
Current site
Google Scholar
PubMed
Close
,
Javier A. Garza-Hernandez Laboratorio Entomología Médica, Instituto de Ciencias Biomédicas, Universidad Autónoma de Ciudad Juárez, Ciudad Juárez, Chihuahua, México;

Search for other papers by Javier A. Garza-Hernandez in
Current site
Google Scholar
PubMed
Close
,
Ma Isabel Salazar Laboratorio de Virología e Inmunovirología, Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de México, Mexico;

Search for other papers by Ma Isabel Salazar in
Current site
Google Scholar
PubMed
Close
,
Erick J. De Luna-Santillana Laboratorio Medicina de la Conservación, Centro de Biotecnología Genómica del Instituto Politécnico Nacional, Reynosa, Tamaulipas, México;

Search for other papers by Erick J. De Luna-Santillana in
Current site
Google Scholar
PubMed
Close
,
Chandra S. Tangudu Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa;

Search for other papers by Chandra S. Tangudu in
Current site
Google Scholar
PubMed
Close
,
Rosa C. Cetina-Trejo Laboratorio de Arbovirología, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autónoma de Yucatán, Mérida, México;

Search for other papers by Rosa C. Cetina-Trejo in
Current site
Google Scholar
PubMed
Close
,
Gloria L. Doria-Cobos Departamento de Epidemiología de la Cuarta Jurisdicción Sanitaria, Secretaria de Salud, Reynosa, Tamaulipas, México;

Search for other papers by Gloria L. Doria-Cobos in
Current site
Google Scholar
PubMed
Close
,
Santos Daniel Carmona-Aguirre Secretaría de Salud del Estado de Tamaulipas, Dirección de Epidemiología, Ciudad Victoria, Tamaulipas, México

Search for other papers by Santos Daniel Carmona-Aguirre in
Current site
Google Scholar
PubMed
Close
,
Julian E. Garcia-Rejon Laboratorio de Arbovirología, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autónoma de Yucatán, Mérida, México;

Search for other papers by Julian E. Garcia-Rejon in
Current site
Google Scholar
PubMed
Close
,
Carlos Machain-Williams Laboratorio de Arbovirología, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autónoma de Yucatán, Mérida, México;

Search for other papers by Carlos Machain-Williams in
Current site
Google Scholar
PubMed
Close
,
Bradley J. Blitvich Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, Iowa;

Search for other papers by Bradley J. Blitvich in
Current site
Google Scholar
PubMed
Close
, and
Mario Alberto Rodríguez Pérez Laboratorio de Biomedicina Molecular, Centro de Biotecnología Genómica del Instituto Politécnico Nacional, Reynosa, Tamaulipas, México;

Search for other papers by Mario Alberto Rodríguez Pérez in
Current site
Google Scholar
PubMed
Close
Restricted access

A clinical, serological, and molecular investigation was performed to determine the presence of dengue virus (DENV) and other flaviviruses among residents of the city of Reynosa, Tamaulipas, on the Mexico–U.S. border in 2014–2016. The sample population consisted of 2,355 patients with suspected dengue, in addition to 346 asymptomatic individuals recruited during a household-based epidemiological investigation designed to identify flavivirus seroconversions. Sera were collected from patients with suspected dengue in the acute phase of illness and from asymptomatic individuals at enrollment and every 5–7 months for 19 months. Sera from suspected dengue patients were tested for DENV antigen by enzyme-linked immunosorbent assay (ELISA), and select antigen-positive sera were further tested using a serotype-specific, quantitative reverse transcription–polymerase chain reaction. Sera from the household cohort were tested for flavivirus-reactive antibodies by immunoglobulin (Ig) M and IgG ELISAs using DENV antigen. A total of 418 (17.7%) patients with suspected dengue had laboratory-confirmed DENV infections, including 82 patients who were positive for DENV RNA. The most frequently detected serotype was DENV-1 (61 patients), followed by DENV-2 (16 patients) and DENV-3 (five patients). A total of 217 (62.7%) asymptomatic individuals had flavivirus-reactive antibodies at enrollment, and nine flavivirus-naïve individuals seroconverted. Sera from a subset of dengue patients and household participants, including all those who seroconverted, were further tested by plaque reduction neutralization test, resulting in the detection of antibodies to DENV-1, DENV-2, and West Nile virus. In summary, we provide evidence for the co-circulation of multiple flaviviruses in Reynosa, Tamaulipas, on the Mexico–U.S. border.

Author Notes

Address correspondence to Bradley J. Blitvich, Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, 2116 Veterinary Medicine Bldg., Ames, IA 50011. E-mail: blitvich@iastate.edu

Financial support: The study was supported by scholarships from the Consejo Nacional de Ciencia y Tecnología of Mexico (scholarship no. 262076) and Coordinación de Cooperación Académica del Instituto Politécnico Nacional of Mexico, and in part by CONACYT grants 2014-247005 and 200664, an intramural grant from Iowa State University, and an institutional grant (Ref. No. CIP-ICB-2018-103) used to support a visiting scholar at the Universidad Autónoma de Ciudad Juárez.

Authors’ addresses: S. Viridiana Laredo-Tiscareño and Erick J. De Luna-Santillana, Centro de Biotecnología Genómica del Instituto Politécnico Nacional, Laboratorio de Biomedicina Molecular, Reynosa, Tamaulipas, México, E-mails: viridiana.laredo@gmail.com and ericklusan@yahoo.com. Javier A. Garza-Hernandez and Mario Alberto Rodríguez Pérez, Centro de Biotecnologia Genomica, Instituto Politecnico Nacional, Mexico, Tamaulipas, México, E-mails: biolgarza@gmail.com and drmarodriguez@hotmail.com. Ma Isabel Salazar, Departamento de Microbiología, Instituto Politécnico Nacional Escuela Nacional de Ciencias Biológicas, Ciudad de México, México, E-mail: maisabelsalazar@gmail.com. Chandra S. Tangudu and Bradley J. Blitvich, Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA, E-mails: ctangudu@iastate.edu and blitvich@iastate.edu. Rosa C. Cetina-Trejo, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autonoma de Yucatan, Merida, Yucatán, México, E-mail: rosaccentinatrejo1234@gmail.com. Gloria L. Doria-Cobos, Epidemiología de la Cuarta Jurisdicción Sanitaria, Secretaria de Salud, Reynosa, Tamaulipas, México, E-mail: leticiaddruiz@gmail.com. Santos Daniel Carmona-Aguirre, Direccion de Epidemiologia, Secretaria de Salud del Estado de Tamaulipas, Ciudad Victoria, Tamaulipas, México, E-mail: santos.carmona@tam.gob.mx. Julian E. Garcia-Rejon, Laboratorio de Arbovirología, Universidad Autonoma de Yucatan, Merida, Yucatán, México, E-mail: julian.garcia.rejon@gmail.com. Carlos Machain-Williams, Hideo Noguchi Institute, Universidad Autónoma de Yucatán, Merida, Yucatán, México, E-mail: carlos.machain@uady.mx.

  • 1.

    Brathwaite Dick O, San Martin JL, Montoya RH, del Diego J, Zambrano B, Dayan GH, 2012. The history of dengue outbreaks in the Americas. Am J Trop Med Hyg 87: 584593.

  • 2.

    Guzman MG, Gubler DJ, Izquierdo A, Martinez E, Halstead SB, 2016. Dengue infection. Nat Rev Dis Primers 2: 16055.

  • 3.

    Murray NE, Quam MB, Wilder-Smith A, 2013. Epidemiology of dengue: past, present and future prospects. Clin Epidemiol 5: 299309.

  • 4.

    Bhatt S et al. 2013. The global distribution and burden of dengue. Nature 496: 504507.

  • 5.

    Undurraga EA et al. 2015. Economic and disease burden of dengue in Mexico. PLoS Negl Trop Dis 9: e0003547.

  • 6.

    World Health Organization, 1997. Dengue Haemorrhagic Fever: Diagnosis, Treatment, Prevention and Control, 2nd edition. Geneva, Switzerland: WHO.

    • PubMed
    • Export Citation
  • 7.

    Balmaseda A, Hammond SN, Perez MA, Cuadra R, Solano S, Rocha J, Idiaquez W, Harris E, 2005. Short report: assessment of the World Health Organization scheme for classification of dengue severity in Nicaragua. Am J Trop Med Hyg 73: 10591062.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Phuong CX et al. 2004. Clinical diagnosis and assessment of severity of confirmed dengue infections in Vietnamese children: is the world health organization classification system helpful? Am J Trop Med Hyg 70: 172179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    World Health Organization, 2009. Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control, New Edition. Geneva, Switzerland: WHO.

    • PubMed
    • Export Citation
  • 10.

    Blitvich BJ, 2008. Transmission dynamics and changing epidemiology of West Nile virus. Anim Health Res Rev 9: 7186.

  • 11.

    Petersen LR, Brault AC, Nasci RS, 2013. West Nile virus: review of the literature. JAMA 310: 308315.

  • 12.

    Reisen WK, 2003. Epidemiology of St. Louis encephalitis virus. Adv Virus Res 61: 139183.

  • 13.

    Oyer RJ, David Beckham J, Tyler KL, 2014. West Nile and St. Louis encephalitis viruses. Handb Clin Neurol 123: 433447.

  • 14.

    Petersen LR, Jamieson DJ, Powers AM, Honein MA, 2016. Zika virus. N Engl J Med 374: 15521563.

  • 15.

    Weaver SC, Costa F, Garcia-Blanco MA, Ko AI, Ribeiro GS, Saade G, Shi PY, Vasilakis N, 2016. Zika virus: history, emergence, biology, and prospects for control. Antiviral Res 130: 6980.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Ibanez-Bernal S, Briseno B, Mutebi JP, Argot E, Rodriguez G, Martinez-Campos C, Paz R, de la Fuente-San Roman P, Tapia-Conyer R, Flisser A, 1997. First record in America of Aedes albopictus naturally infected with dengue virus during the 1995 outbreak at Reynosa, Mexico. Med Vet Entomol 11: 305309.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Rawlings J et al. 1996. Dengue fever at the US-Mexico border, 1995–1996 (reprinted from MMWR, vol 45, pg 841, 1996). JAMA 276: 14641465.

  • 18.

    Ramos MM et al. 2008. Epidemic dengue and dengue hemorrhagic fever at the Texas-Mexico border: results of a household-based seroepidemiologic survey, December 2005. Am J Trop Med Hyg 78: 364369.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Brunkard JM, Robles Lopez JL, Ramirez J, Cifuentes E, Rothenberg SJ, Hunsperger EA, Moore CG, Brussolo RM, Villarreal NA, Haddad BM, 2007. Dengue fever seroprevalence and risk factors, Texas-Mexico border, 2004. Emerg Infect Dis 13: 14771483.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Thomas DL et al. 2016. Reemergence of dengue in southern Texas, 2013. Emerg Infect Dis 22: 10021007.

  • 21.

    Secretaría de Salud México, Boletín Epidemiológico SNdVESÚdI, 2015. Available at: https://www.gob.mx/cms/uploads/attachment/file/10564/sem27.pdf. Accessed January 1, 2018.

    • PubMed
    • Export Citation
  • 22.

    Secretaria de Salud, 2015. Lineamientos para la Vigilancia Epidemiológica de Dengue por Laboratorio (Guidelines for Epidemiological Surveillance of Dengue in the Laboratory). Available at: https://www.gob.mx/cms/uploads/attachment/file/23789/Lineamientos_para_la_vigilancia_epidemiologica_de_dengue.pdf. Accessed April 9, 2018.

    • PubMed
    • Export Citation
  • 23.

    Chien LJ, Liao TL, Shu PY, Huang JH, Gubler DJ, Chang GJ, 2006. Development of real-time reverse transcriptase PCR assays to detect and serotype dengue viruses. J Clin Microbiol 44: 12951304.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Beaty B, Calisher C, Shope R, 1995. Arboviruses. Lennette E, Lennette D, Lennette E, eds. Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections. Washington, DC: American Public Health Association, 189–212.

    • PubMed
    • Export Citation
  • 25.

    Chappell WA, Sasso DR, Toole RF, Monath TP, 1971. Labile serum factor and its effect on arbovirus neutralization. Appl Microbiol 21: 7983.

  • 26.

    Laredo-Tiscareño SV et al. 2018. Arbovirus surveillance near the Mexico-U.S. border: isolation and sequence analysis of chikungunya virus from patients with dengue-like symptoms in Reynosa, Tamaulipas. Am J Trop Med Hyg 99: 191194.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Leduc-Galindo D et al. 2015. Characterization of the dengue outbreak in Nuevo Leon state, Mexico, 2010. Infection 43: 201206.

  • 28.

    Dantes HG, Farfan-Ale JA, Sarti E, 2014. Epidemiological trends of dengue disease in Mexico (2000–2011): a systematic literature search and analysis. PLoS Negl Trop Dis 8: e3158.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Shrivastava S, Tiraki D, Diwan A, Lalwani SK, Modak M, Mishra AC, Arankalle VA, 2018. Co-circulation of all the four dengue virus serotypes and detection of a novel clade of DENV-4 (genotype I) virus in Pune, India during 2016 season. PLoS One 13: e0192672.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Andrade EH et al. 2016. Spatial-temporal co-circulation of dengue virus 1, 2, 3, and 4 associated with coinfection cases in a hyperendemic area of Brazil: a 4-week survey. Am J Trop Med Hyg 94: 10801084.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Endy TP, Nisalak A, Chunsuttiwat S, Libraty DH, Green S, Rothman AL, Vaughn DW, Ennis FA, 2002. Spatial and temporal circulation of dengue virus serotypes: a prospective study of primary school children in Kamphaeng Phet, Thailand. Am J Epidemiol 156: 5259.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Castonguay-Vanier J et al. 2018. Molecular epidemiology of dengue viruses in three provinces of Lao PDR, 2006–2010. PLoS Negl Trop Dis 12: e0006203.

  • 33.

    Caron M, Grard G, Paupy C, Mombo IM, Bikie Bi Nso B, Kassa Kassa FR, Nkoghe D, Leroy EM, 2013. First evidence of simultaneous circulation of three different dengue virus serotypes in Africa. PLoS One 8: e78030.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Ridde V, Agier I, Bonnet E, Carabali M, Dabire KR, Fournet F, Ly A, Meda IB, Parra B, 2016. Presence of three dengue serotypes in Ouagadougou (Burkina Faso): research and public health implications. Infect Dis Poverty 5: 23.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    De Simone TS, Nogueira RM, Araujo ES, Guimaraes FR, Santos FB, Schatzmayr HG, Souza RV, Teixeira Filho G, Miagostovich MP, 2004. Dengue virus surveillance: the co-circulation of DENV-1, DENV-2 and DENV-3 in the state of Rio de Janeiro, Brazil. Trans R Soc Trop Med Hyg 98: 553562.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Humayoun MA, Waseem T, Jawa AA, Hashmi MS, Akram J, 2010. Multiple dengue serotypes and high frequency of dengue hemorrhagic fever at two tertiary care hospitals in Lahore during the 2008 dengue virus outbreak in Punjab, Pakistan. Int J Infect Dis 14: E54E59.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Lorono-Pino MA, Cropp CB, Farfan JA, Vorndam AV, Rodriguez-Angulo EM, Rosado-Paredes EP, Flores-Flores LF, Beaty BJ, Gubler DJ, 1999. Common occurrence of concurrent infections by multiple dengue virus serotypes. Am J Trop Med Hyg 61: 725730.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Jones JM et al. 2016. Binational dengue outbreak along the United States-Mexico border—Yuma County, Arizona, and Sonora, Mexico, 2014. MMWR Morb Mortal Wkly Rep 65: 495499.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Centers for Disease Control and Prevention, 2007. Dengue hemorrhagic fever–U.S.-Mexico border, 2005. MMWR Morb Mortal Wkly Rep 56: 785789.

  • 40.

    Lorono-Pino MA et al. 2004. Introduction of the American/Asian genotype of dengue 2 virus into the Yucatan state of Mexico. Am J Trop Med Hyg 71: 485492.

  • 41.

    Gunther J, Ramirez-Palacio LR, Perez-Ishiwara DG, Salas-Benito JS, 2009. Distribution of dengue cases in the state of Oaxaca, Mexico, during the period 2004–2006. J Clin Virol 45: 218222.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Rodriguez Mde L et al. 2010. Serologic surveillance for West Nile virus and other flaviviruses in febrile patients, encephalitic patients, and asymptomatic blood donors in northern Mexico. Vector Borne Zoonotic Dis 10: 151157.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Centers for Disease Control and Prevention. ArboNet, Dengue Virus (Locally Acquired and Imported). Available at: https://wwwn.cdc.gov/arbonet/maps/ADB_Diseases_Map/index.html. Accessed April 24, 2018.

    • PubMed
    • Export Citation
  • 44.

    Reiter P et al. 2003. Texas lifestyle limits transmission of dengue virus. Emerg Infect Dis 9: 8689.

  • 45.

    Clark GG, 2008. Dengue and dengue hemorrhagic fever in northern Mexico and south Texas: do they really respect the border? Am J Trop Med Hyg 78: 361362.

  • 46.

    Brunkard JM, Cifuentes E, Rothenberg SJ, 2008. Assessing the roles of temperature, precipitation, and ENSO in dengue re-emergence on the Texas-Mexico border region. Salud Publica Mex 50: 227234.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Elizondo-Quiroga D et al. 2005. West Nile virus isolation in human and mosquitoes, Mexico. Emerg Infect Dis 11: 14491452.

  • 48.

    Rios-Ibarra C, Blitvich BJ, Farfan-Ale J, Ramos-Jimenez J, Muro-Escobedo S, Martinez-Rodriguez HR, OrtizLopez R, Torres-Lopez E, Rivas-Estilla AM, 2010. Fatal human case of West Nile disease, Mexico, 2009. Emerg Infect Dis 16: 741743.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Fernandez-Salas I et al. 2003. Serologic evidence of West Nile virus infection in birds, Tamaulipas state, Mexico. Vector Borne Zoonotic Dis 3: 209213.

  • 50.

    Blitvich BJ et al. 2004. Phylogenetic analysis of West Nile virus, Nuevo Leon state, Mexico. Emerg Infect Dis 10: 13141317.

  • 51.

    Ibarra-Juarez L, Eisen L, Bolling BG, Beaty BJ, Blitvich BJ, Sanchez-Casas RM, Ayala-Sulca YO, Fernandez-Salas I, 2012. Detection of West Nile virus-specific antibodies and nucleic acid in horses and mosquitoes, respectively, in Nuevo Leon state, northern Mexico, 2006–2007. Med Vet Entomol 26: 351354.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Blitvich BJ, Fernandez-Salas I, Contreras-Cordero JF, Marlenee NL, Gonzalez-Rojas JI, Komar N, Gubler DJ, Calisher CH, Beaty BJ, 2003. Serologic evidence of West Nile virus infection in horses, Coahuila state, Mexico. Emerg Infect Dis 9: 853856.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Deardorff E et al. 2006. Introductions of West Nile virus strains to Mexico. Emerg Infect Dis 12: 314318.

  • 54.

    Estrada-Franco JG et al. 2003. West Nile virus in Mexico: evidence of widespread circulation since July 2002. Emerg Infect Dis 9: 16041607.

  • 55.

    World Health Organization. Zika Virus Infection—Mexico. Geneva, Switzerland: WHO. Available at: http://www.who.int/csr/don/03-december-2015-zika-mexico/en/. Accessed May 5, 2018.

    • PubMed
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 139 119 10
Full Text Views 502 13 2
PDF Downloads 217 3 2
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save