Epidemiological and ecological determinants of Zika virus transmission in an urban setting

  1. José Lourenço  Is a corresponding author
  2. Maricelia Maia de Lima
  3. Nuno Rodrigues Faria
  4. Andrew Walker
  5. Moritz UG Kraemer
  6. Christian Julian Villabona-Arenas
  7. Ben Lambert
  8. Erenilde Marques de Cerqueira
  9. Oliver G Pybus
  10. Luiz CJ Alcantara
  11. Mario Recker
  1. University of Oxford, United Kingdom
  2. FIOCRUZ, Brazil
  3. Université de Montpellier, France
  4. Centre of PostGraduation in Collective Health, Universidade Estadual de Feira de Santana, Brazil
  5. University of Exeter, United Kingdom

Abstract

The Zika virus has emerged as a global public health concern. Its rapid geographic expansion is attributed to the success of Aedes mosquito vectors, but local epidemiological drivers are still poorly understood. Feira de Santana played a pivotal role in the Chikungunya epidemic in Brazil and was one of the first urban centres to report Zika infections. Using a climate-driven transmission model and notified Zika case data, we show that a low observation rate and high vectorial capacity translated into a significant attack rate during the 2015 outbreak, with a subsequent decline in 2016 and fade-out in 2017 due to herd-immunity. We find a potential Zika-related, low risk for microcephaly per pregnancy, but with significant public health impact given high attack rates. The balance between the loss of herd-immunity and viral re-importation will dictate future transmission potential of in this urban setting.

Article and author information

Author details

  1. José Lourenço

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    For correspondence
    jose.lourenco@zoo.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9318-2581
  2. Maricelia Maia de Lima

    Laboratory of Haematology, Genetics and Computational Biology, FIOCRUZ, Salvador, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  3. Nuno Rodrigues Faria

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8839-2798
  4. Andrew Walker

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Moritz UG Kraemer

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8838-7147
  6. Christian Julian Villabona-Arenas

    Institut de Recherche pour le Développement (IRD), UMI 233, INSERM U1175, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9928-3968
  7. Ben Lambert

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Erenilde Marques de Cerqueira

    Department of Health, Centre of PostGraduation in Collective Health, Universidade Estadual de Feira de Santana, Feira de Santana, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  9. Oliver G Pybus

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Luiz CJ Alcantara

    Laboratory of Haematology, Genetics and Computational Biology, FIOCRUZ, Salvador, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  11. Mario Recker

    Centre for Mathematics and the Environment, University of Exeter, Penryn, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9489-1315

Funding

European Research Council (614725-PATHPHYLODYN)

  • Oliver G Pybus

Royal Society

  • Mario Recker

Wellcome Trust & Royal Society (204311/Z/16/Z)

  • Nuno Rodrigues Faria

Engineering and Physical Sciences Research Council

  • Ben Lambert

European Research Council (268904 - DIVERSITY)

  • José Lourenço
  • Andrew Walker

International Development Emerging Pandemic Threats Program-2 (AID-OAA-A-14-00102)

  • Moritz UG Kraemer

Labex EpiGenMed (ANR-10-LABX-12-01)

  • Christian Julian Villabona-Arenas

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mark Jit, London School of Hygiene & Tropical Medicine, and Public Health England, United Kingdom

Version history

  1. Received: June 21, 2017
  2. Accepted: September 4, 2017
  3. Accepted Manuscript published: September 9, 2017 (version 1)
  4. Version of Record published: October 12, 2017 (version 2)

Copyright

© 2017, Lourenço et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. José Lourenço
  2. Maricelia Maia de Lima
  3. Nuno Rodrigues Faria
  4. Andrew Walker
  5. Moritz UG Kraemer
  6. Christian Julian Villabona-Arenas
  7. Ben Lambert
  8. Erenilde Marques de Cerqueira
  9. Oliver G Pybus
  10. Luiz CJ Alcantara
  11. Mario Recker
(2017)
Epidemiological and ecological determinants of Zika virus transmission in an urban setting
eLife 6:e29820.
https://doi.org/10.7554/eLife.29820

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    Background: High levels of circulating adiponectin are associated with increased insulin sensitivity, low prevalence of diabetes, and low body mass index (BMI); however, high levels of circulating adiponectin are also associated with increased mortality in the 60-70 age group. In this study, we aimed to clarify factors associated with circulating high-molecular-weight (cHMW) adiponectin levels and their association with mortality in the very old (85-89 years old) and centenarians.

    Methods: The study included 812 (women: 84.4%) for centenarians and 1,498 (women: 51.7%) for the very old. The genomic DNA sequence data were obtained by whole genome sequencing or DNA microarray-imputation methods. LASSO and multivariate regression analyses were used to evaluate cHMW adiponectin characteristics and associated factors. All-cause mortality was analyzed in three quantile groups of cHMW adiponectin levels using Cox regression.

    Results: The cHMW adiponectin levels were increased significantly beyond 100 years of age, were negatively associated with diabetes prevalence, and were associated with SNVs in CDH13 (p = 2.21 × 10-22) and ADIPOQ (p = 5.72 × 10-7). Multivariate regression analysis revealed that genetic variants, BMI, and high-density lipoprotein cholesterol (HDLC) were the main factors associated with cHMW adiponectin levels in the very old, whereas the BMI showed no association in centenarians. The hazard ratios for all-cause mortality in the intermediate and high cHMW adiponectin groups in very old men were significantly higher rather than those for all-cause mortality in the low level cHMW adiponectin group, even after adjustment with BMI. In contrast, the hazard ratios for all-cause mortality were significantly higher for high cHMW adiponectin groups in very old women, but were not significant after adjustment with BMI.

    Conclusions: cHMW adiponectin levels increased with age until centenarians, and the contribution of known major factors associated with cHMW adiponectin levels, including BMI and HDLC, varies with age, suggesting that its physiological significance also varies with age in the oldest old.

    Funding: This study was supported by grants from the Ministry of Health, Welfare, and Labour for the Scientific Research Projects for Longevity; a Grant-in-Aid for Scientific Research (No 21590775, 24590898, 15KT0009, 18H03055, 20K20409, 20K07792, 23H03337) from the Japan Society for the Promotion of Science; Keio University Global Research Institute (KGRI), Kanagawa Institute of Industrial Science and Technology (KISTEC), Japan Science and Technology Agency (JST) Research Complex Program 'Tonomachi Research Complex' Wellbeing Research Campus: Creating new values through technological and social innovation (JP15667051), the Program for an Integrated Database of Clinical and Genomic Information from the Japan Agency for Medical Research and Development (No. 16kk0205009h001, 17jm0210051h0001, 19dk0207045h0001); the medical-welfare-food-agriculture collaborative consortium project from the Japan Ministry of Agriculture, Forestry, and Fisheries; and the Biobank Japan Program from the Ministry of Education, Culture, Sports, and Technology.