Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
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Baud D , Gubler DJ , Schaub B , Lanteri MC , Musso D , 2017. An update on Zika virus infection. Lancet 390: 2099–2109.
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Espinal MA , Andrus JK , Jauregui B , Waterman SH , Morens DM , Santos JI , Horstick O , Francis LA , Olson D , 2019. Emerging and reemerging Aedes-transmitted arbovirus infections in the region of the Americas: implications for health policy. Am J Public Health 109: 387–392.
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9.
Castillo Signor LDC , Edwards T , Escobar LE , Mencos Y , Matope A , Castaneda-Guzman M , Adams ER , Cuevas LE , 2020. Epidemiology of dengue fever in Guatemala. PLoS Negl Trop Dis 14: e0008535.
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Ferraris P , Yssel H , Missé D , 2019. Zika virus infection: an update. Microbes Infect 21: 353–360.
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Imai N , Ferguson NM , 2018. Targeting vaccinations for the licensed dengue vaccine: Considerations for serosurvey design. PLoS One 13: e0199450.
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14.
Fritzell C , Rousset D , Adde A , Kazanji M , Van Kerkhove MD , Flamand C , 2018. Current challenges and implications for dengue, chikungunya and Zika seroprevalence studies worldwide: a scoping review. PLoS Negl Trop Dis 12: e0006533.
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15.
Nealon J , Bouckenooghe A , Cortes M , Coudeville L , Frago C , Macina D , Tam CC , 2022. Dengue endemicity, force of infection, and variation in transmission intensity in 13 endemic countries. J Infect Dis 225: 75–83.
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Asturias EJ et al., 2016. The Center for Human Development in Guatemala: an innovative model for global population health. Adv Pediatr 63: 357–387.
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17.
Departamento de Epidemiología, Ministerio de Salud Pública y Asistencia Social INdE, Secretaría de Planificación y Programación de la Presidencia , 2021. Situación Epidemiológica de las Arbovirosis en Guatemala. Available at: http://epidemiologia.mspas.gob.gt/files/2021/salas-situacionales/arbovirosis/ARB-SE-13-2021.pdf. Accessed May 12, 2022.
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Singh J , Jain DC , Sharma RS , Verghese T , 1996. Evaluation of immunization coverage by lot quality assurance sampling compared with 30-cluster sampling in a primary health centre in India. Bull World Health Organ 74: 269–274.
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D’Ardenne KK , Darrow J , Furniss A , Chavez C , Hernandez H , Berman S , Asturias EJ , 2016. Use of rapid needs assessment as a tool to identify vaccination delays in Guatemala and Peru. Vaccine 34: 1719–1725.
-
20.
Lanata CF , Black RE , 1991. Lot quality assurance sampling techniques in health surveys in developing countries: advantages and current constraints. World Health Stat Q 44: 133–139.
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21.
Malilay J , Flanders WD , Brogan D , 1996. A modified cluster-sampling method for post-disaster rapid assessment of needs. Bull World Health Organ 74: 399–405.
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World Health Organization , 2005. Immunization Coverage Cluster Survey Reference Manual. Geneva, Switzerland: WHO.
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23.
Henderson RH , Sundaresan T , 1982. Cluster sampling to assess immunization coverage: a review of experience with a simplified sampling method. Bull World Health Organ 60: 253–260.
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Olson D et al., 2017. Performance of a mobile phone app-based participatory syndromic surveillance system for acute febrile illness and acute gastroenteritis in rural Guatemala. J Med Internet Res 19: e368.
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25.
Olson D , Lamb MM , Lopez MR , Paniagua-Avila MA , Zacarias A , Samayoa-Reyes G , Cordon-Rosales C , Asturias EJ , 2017. A rapid epidemiological tool to measure the burden of norovirus infection and disease in resource-limited settings. Open Forum Infect Dis 4: ofx049.
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Repeated Rapid Active Sampling Surveys Demonstrated a Rapidly Changing Zika Seroprevalence among Children in a Rural Dengue-endemic Region in Southwest Guatemala during the Zika Epidemic (2015–2016)
Molly M. Lamb
Molly M. Lamb
Department of Epidemiology and Center for Global Health, Colorado School of Public Health, Aurora, Colorado;
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Alejandra Paniagua-Avila
Alejandra Paniagua-Avila
Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, New York;
Center for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;
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Center for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;
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Alma Zacarias
Alma Zacarias
Center for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;
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Neudy Rojop
Neudy Rojop
Center for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;
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Andrea Chacon
Andrea Chacon
Center for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;
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Muktha S. Natrajan
Muktha S. Natrajan
Emory University Department of Medicine, Division of Infectious Diseases, Atlanta, Georgia;
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Jesse J. Waggoner
Jesse J. Waggoner
Emory University Department of Medicine, Division of Infectious Diseases, Atlanta, Georgia;
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Maria Renee Lopez
Maria Renee Lopez
Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala City, Guatemala;
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Celia Cordon-Rosales
Celia Cordon-Rosales
Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala City, Guatemala;
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James W. Huleatt
James W. Huleatt
Sanofi, Swiftwater, Pennsylvania;
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Matthew I. Bonaparte
Matthew I. Bonaparte
Sanofi, Swiftwater, Pennsylvania;
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Edwin J. Asturias
Edwin J. Asturias
Department of Epidemiology and Center for Global Health, Colorado School of Public Health, Aurora, Colorado;
Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colorado
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Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colorado
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Daniel Olson
Daniel Olson
Department of Epidemiology and Center for Global Health, Colorado School of Public Health, Aurora, Colorado;
Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colorado
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Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colorado
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ABSTRACT.
Although Central America is largely dengue virus (DENV)-endemic, the 2015–2016 Zika virus (ZIKV) pandemic brought new urgency to develop surveillance approaches capable of characterizing the rapidly changing disease burden in resource-limited settings. We conducted a pediatric DENV surveillance study in rural Guatemala, including serial cross-sectional surveys from April through September 2015 (Survey 1), in October–November 2015 (Survey 2), and January–February 2016 (Survey 3). Serum underwent DENV IgM MAC ELISA and polymerase chain reaction testing. Using banked specimens from Surveys 2 and 3, we expanded testing to include DENV 1–4 and ZIKV microneutralization (MN50), DENV NS1 IgG ELISA, and ZIKV anti-NS1 antibody Blockage of Binding (BoB) ELISA testing. Demographic risk factors for ZIKV BoB positivity were explored using multivariable generalized linear regression models. Of Survey 2 and 3 samples available (N = 382), DENV seroprevalence slightly increased (+1%–10% depending on the assay) during the surveillance period and increased with age. In contrast, ZIKV seroprevalence consistently increased over the 3-month period, including from 6% to 34% (P < 0.0001) and 10%–37% (P < 0.0001) using the MN50 ≥100 and BoB ELISA assays, respectively. Independent risk factors for ZIKV seropositivity included older age (prevalence ratio (PR)/year = 1.12, 95% confidence interval (CI) = 1.07–1.17) and primary caregiver literacy (PR = 2.80, CI = 1.30–6.06). Rapid active surveillance (RAS) surveys demonstrated a nearly 30% increase in ZIKV prevalence and a slight (≤ 10%) increase in DENV seroprevalence from October to November 2015 to January to February 2016 in rural southwest Guatemala, regardless of serologic assay used. RAS surveys may be a useful “off-the-shelf” tool to characterize arboviruses and other emerging pathogens rapidly in resource-limited settings.
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Author Notes
Funding information: This study was supported by an Investigator-Initiated Sponsored Research Grant from Takeda Pharmaceuticals (IISR-2014-100647) and a Material Transfer Agreement with Sanofi. D. O. is supported by NIH/National Center for Advancing Translational Sciences Colorado CTSI (Clinical and Translational Sciences Institute) grant no. UL1 TR001082 and National Institute of Allergy and Infectious Diseases grant no. 1K23AI143967-01. Contents are the authors’ sole responsibility and do not necessarily represent official NIH view.
Disclosure: Dr. Lamb is partially supported by grants from Roche, Pfizer, and Biofire. Dr. Asturias has research support from Pfizer and serves on the data safety monitoring boards of Curevax and Inovio. Dr. Olson is partially supported by grants from Roche and Pfizer. James Huleatt and Matthew Bonaparte are Sanofi employees and may or may not hold company stocks.
Authors’ addresses: Molly M. Lamb, Department of Epidemiology and Center for Global Health, Colorado School of Public Health, Aurora, CO, E-mail: Molly.Lamb@cuanschutz.edu. Alejandra Paniagua-Avila, Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, and Center for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala, E-mail: malejandrapaniagua@gmail.com. Alma Zacarias, Neudy Rojop, and Andrea Chacon, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala, E-mails: almaloarca@yahoo.es, neudy.rojop.fsigcu@gmail.com, and chaconjuarez@gmail.com. Muktha S. Natrajan and Jesse J. Waggoner, Emory University Department of Medicine, Division of Infectious Diseases, Atlanta, GA, E-mails: qdz9@cdc.gov and jesse.waggoner@emoryhealthcare.org. Maria Renee Lopez and Celia Cordon-Rosales, Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala City, Guatemala, E-mails: mlopez@ces.uvg.edu.gt and ccordon@ces.uvg.edu.gt. James W. Huleatt and Matthew I. Bonaparte, Sanofi, Swiftwater, Pennsylvania, E-mails: James.Huleatt@sanofi.com and Matthew.Bonaparte@sanofi.com. Edwin J. Asturias and Daniel Olson, Department of Epidemiology and Center for Global Health, Colorado School of Public Health, Aurora, CO, and Department of Pediatrics, University of Colorado School of Medicine, Aurora, CO E-mails: Edwin.Asturias@childrenscolorado.org and Daniel.Olson@childrenscolorado.org.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Bhatt S et al., 2013. The global distribution and burden of dengue. Nature 496: 504–507.
-
2.
World Health Organization , 2009. Dengue: guidelines for diagnosis, treatment, prevention and control. Geneva, Switzerland: WHO.
-
3.
Cattarino L , Rodriguez-Barraquer I , Imai N , Cummings DAT , Ferguson NM , 2020. Mapping global variation in dengue transmission intensity. Sci Transl Med 12: eaaax4144.
-
4.
Moore CA et al., 2017. Characterizing the pattern of anomalies in congenital zika syndrome for pediatric clinicians. JAMA Pediatr 171: 288–295.
-
5.
Baud D , Gubler DJ , Schaub B , Lanteri MC , Musso D , 2017. An update on Zika virus infection. Lancet 390: 2099–2109.
-
6.
Espinal MA , Andrus JK , Jauregui B , Waterman SH , Morens DM , Santos JI , Horstick O , Francis LA , Olson D , 2019. Emerging and reemerging Aedes-transmitted arbovirus infections in the region of the Americas: implications for health policy. Am J Public Health 109: 387–392.
-
7.
Theze J et al., 2018. Genomic epidemiology reconstructs the introduction and spread of Zika virus in Central America and Mexico. Cell Host Microbe 23: 855–864 e7.
-
8.
Pielnaa P , Al-Saadawe M , Saro A , Dama MF , Zhou M , Huang Y , Huang J , Xia Z , 2020. Zika virus-spread, epidemiology, genome, transmission cycle, clinical manifestation, associated challenges, vaccine and antiviral drug development. Virology 543: 34–42.
-
9.
Castillo Signor LDC , Edwards T , Escobar LE , Mencos Y , Matope A , Castaneda-Guzman M , Adams ER , Cuevas LE , 2020. Epidemiology of dengue fever in Guatemala. PLoS Negl Trop Dis 14: e0008535.
-
10.
Strategic Advisory Group of Experts on Immunization , 2018. Revised SAGE Recommendation on Use of Dengue vaccine Is Issued. Available at: https://www.infectioncontroltoday.com/view/revised-sage-recommendation-use-dengue-vaccine-issued.
-
11.
Ferraris P , Yssel H , Missé D , 2019. Zika virus infection: an update. Microbes Infect 21: 353–360.
-
12.
Pan YH et al., 2021. Use of seroprevalence to guide dengue vaccination plans for older adults in a dengue non-endemic country. PLoS Negl Trop Dis 15: e0009312.
-
13.
Imai N , Ferguson NM , 2018. Targeting vaccinations for the licensed dengue vaccine: Considerations for serosurvey design. PLoS One 13: e0199450.
-
14.
Fritzell C , Rousset D , Adde A , Kazanji M , Van Kerkhove MD , Flamand C , 2018. Current challenges and implications for dengue, chikungunya and Zika seroprevalence studies worldwide: a scoping review. PLoS Negl Trop Dis 12: e0006533.
-
15.
Nealon J , Bouckenooghe A , Cortes M , Coudeville L , Frago C , Macina D , Tam CC , 2022. Dengue endemicity, force of infection, and variation in transmission intensity in 13 endemic countries. J Infect Dis 225: 75–83.
-
16.
Asturias EJ et al., 2016. The Center for Human Development in Guatemala: an innovative model for global population health. Adv Pediatr 63: 357–387.
-
17.
Departamento de Epidemiología, Ministerio de Salud Pública y Asistencia Social INdE, Secretaría de Planificación y Programación de la Presidencia , 2021. Situación Epidemiológica de las Arbovirosis en Guatemala. Available at: http://epidemiologia.mspas.gob.gt/files/2021/salas-situacionales/arbovirosis/ARB-SE-13-2021.pdf. Accessed May 12, 2022.
-
18.
Singh J , Jain DC , Sharma RS , Verghese T , 1996. Evaluation of immunization coverage by lot quality assurance sampling compared with 30-cluster sampling in a primary health centre in India. Bull World Health Organ 74: 269–274.
-
19.
D’Ardenne KK , Darrow J , Furniss A , Chavez C , Hernandez H , Berman S , Asturias EJ , 2016. Use of rapid needs assessment as a tool to identify vaccination delays in Guatemala and Peru. Vaccine 34: 1719–1725.
-
20.
Lanata CF , Black RE , 1991. Lot quality assurance sampling techniques in health surveys in developing countries: advantages and current constraints. World Health Stat Q 44: 133–139.
-
21.
Malilay J , Flanders WD , Brogan D , 1996. A modified cluster-sampling method for post-disaster rapid assessment of needs. Bull World Health Organ 74: 399–405.
-
22.
World Health Organization , 2005. Immunization Coverage Cluster Survey Reference Manual. Geneva, Switzerland: WHO.
-
23.
Henderson RH , Sundaresan T , 1982. Cluster sampling to assess immunization coverage: a review of experience with a simplified sampling method. Bull World Health Organ 60: 253–260.
-
24.
Olson D et al., 2017. Performance of a mobile phone app-based participatory syndromic surveillance system for acute febrile illness and acute gastroenteritis in rural Guatemala. J Med Internet Res 19: e368.
-
25.
Olson D , Lamb MM , Lopez MR , Paniagua-Avila MA , Zacarias A , Samayoa-Reyes G , Cordon-Rosales C , Asturias EJ , 2017. A rapid epidemiological tool to measure the burden of norovirus infection and disease in resource-limited settings. Open Forum Infect Dis 4: ofx049.
-
26.
Johnson BW , Russell BJ , Lanciotti RS , 2005. Serotype-specific detection of dengue viruses in a fourplex real-time reverse transcriptase PCR assay. J Clin Microbiol 43: 4977–4983.
-
27.
Namekar M , Ellis EM , O’Connell M , Elm J , Gurary A , Park SY , Imrie A , Nerurkar VR , 2013. Evaluation of a new commercially available immunoglobulin M capture enzyme-linked immunosorbent assay for diagnosis of dengue virus infection. J Clin Microbiol 51: 3102–3106.
-
28.
Nascimento EJM , Bonaparte MI , Luo P , Vincent TS , Hu B , George JK , Anez G , Noriega F , Zheng L , Huleatt JW , 2019. Use of a Blockade-of-Binding ELISA and microneutralization assay to evaluate Zika virus serostatus in Dengue-endemic areas. Am J Trop Med Hyg 101: 708–715.
-
29.
Montoya M et al., 2018. Longitudinal analysis of antibody cross-neutralization following Zika virus and Dengue virus infection in Asia and the Americas. J Infect Dis 218: 536–545.
-
30.
Netto EM et al., 2017. High Zika virus seroprevalence in Salvador, northeastern Brazil limits the potential for further outbreaks. MBio 8: https://doi.org/10.1128/mBio.01390-17.
-
31.
Saba Villarroel PM et al., 2018. Zika virus epidemiology in Bolivia: a seroprevalence study in volunteer blood donors. PLoS Negl Trop Dis 12: e0006239.
-
32.
Zambrana JV et al., 2018. Seroprevalence, risk factor, and spatial analyses of Zika virus infection after the 2016 epidemic in Managua, Nicaragua. Proc Natl Acad Sci USA 115: 9294–9299.
-
33.
Diaz-Quinonez JA , Lopez-Martinez I , Torres-Longoria B , Vazquez-Pichardo M , Cruz-Ramirez E , Ramirez-Gonzalez JE , Ruiz-Matus C , Kuri-Morales P , 2016. Evidence of the presence of the Zika virus in Mexico since early 2015. Virus Genes 52: 855–857.
-
34.
Guerbois M et al., 2016. Outbreak of Zika virus infection, Chiapas State, Mexico, 2015, and first confirmed transmission by Aedes aegypti mosquitoes in the Americas. J Infect Dis 214: 1349–1356.
-
35.
Bosch I et al., 2017. Rapid antigen tests for dengue virus serotypes and Zika virus in patient serum. Sci Transl Med 9: eaan1589.
-
36.
Faria NR et al., 2016. Zika virus in the Americas: early epidemiological and genetic findings. Science 352: 345–349.
-
37.
Grubaugh ND et al., 2017. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 546: 401–405.
-
38.
Metsky HC et al., 2017. Zika virus evolution and spread in the Americas. Nature 546: 411–415.
-
39.
Stettler K et al., 2016. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353: 823–826.
-
40.
Velasco-Salas ZI , Sierra GM , Guzman DM , Zambrano J , Vivas D , Comach G , Wilschut JC , Tami A , 2014. Dengue seroprevalence and risk factors for past and recent viral transmission in Venezuela: a comprehensive community-based study. Am J Trop Med Hyg 91: 1039–1048.
-
41.
Pavia-Ruz N et al., 2018. Dengue seroprevalence in a cohort of schoolchildren and their siblings in Yucatan, Mexico (2015–2016). PLoS Negl Trop Dis 12: e0006748.
-
42.
Cheong WH , 1967. Preferred Aedes aegypti larval habitats in urban areas. Bull World Health Organ 36: 586–589.
-
43.
Centers for Disease Control and Prevention , 2020. Community Assessment for Public Health Emergency Response (CASPER). Available at: https://www.cdc.gov/nceh/casper/sampling-methodology.htm. Accessed June 9, 2020.
-
44.
Schnall A , Nakata N , Talbert T , Bayleyegn T , Martinez D , Wolkin A , 2017. Community Assessment for Public Health Emergency Response (CASPER): an innovative emergency management tool in the United States. Am J Public Health 107: S186–S192.
-
45.
Martinez Viedma MDP et al., 2021. Evaluation of ELISA-Based Multiplex Peptides for the Detection of Human Serum Antibodies Induced by Zika Virus Infection across Various Countries. Viruses 13: 1319.
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46.
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