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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. LambDepartment of Epidemiology and Center for Global Health, Colorado School of Public Health, Aurora, Colorado;

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Alejandra Paniagua-AvilaDepartment 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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Alma ZacariasCenter for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;

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Neudy RojopCenter for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;

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Andrea ChaconCenter for Human Development, Fundacion para la Salud Integral de los Guatemaltecos, FUNSALUD, Coatepeque, Quetzaltenango, Guatemala;

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Muktha S. NatrajanEmory University Department of Medicine, Division of Infectious Diseases, Atlanta, Georgia;

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Jesse J. WaggonerEmory University Department of Medicine, Division of Infectious Diseases, Atlanta, Georgia;

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Maria Renee LopezCentro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala City, Guatemala;

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Celia Cordon-RosalesCentro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala City, Guatemala;

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James W. HuleattSanofi, Swiftwater, Pennsylvania;

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Matthew I. BonaparteSanofi, Swiftwater, Pennsylvania;

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Edwin J. AsturiasDepartment 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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Daniel OlsonDepartment 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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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

Address correspondence to Daniel Olson, Department of Pediatrics, Center for Global Health, University of Colorado School of Medicine, 13199 E. Montview Blvd, Suite 310, Aurora, CO 80045. E-mail: Daniel.Olson@cuanschutz.edu

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.

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