Incubation Periods of Mosquito-Borne Viral Infections: A Systematic Review

Am. J. Trop. Med. Hyg., 90(5), 2014, pp. 882–891 doi:10.4269/ajtmh.13-0403 Copyright © 2014 by The American Society of Tropical Medicine and Hygiene Review Article: Incubation Periods of Mosquito-Borne Viral Infections: A Systematic Review Kara E. Rudolph, Justin Lessler,* Rachael M. Moloney, Brittany Kmush, and Derek A. T. Cummings Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland Abstract. Mosquito-borne viruses are a major public health threat, but their incubation periods are typically uncited, non-specific, and not based on data. We systematically review the published literature on six mosquito-borne viruses selected for their public health importance: chikungunya, dengue, Japanese encephalitis, Rift Valley fever, West Nile, and yellow fever viruses. For each, we identify the literature’s consensus on the incubation period, evaluate the evidence for this consensus, and provide detailed estimates of the incubation period and distribution based on published experimental and observational data. We abstract original data as doubly interval-censored observations. Assuming a log-normal distribution, we estimate the median incubation period, dispersion, 25th and 75th percentiles by maximum likelihood. We include bootstrapped 95% confidence intervals for each estimate. For West Nile and yellow fever viruses, we also estimate the 5th and 95th percentiles of their incubation periods. B Encephalitis, JE, JEV, JBE, West Nile, WN, WNV, Rift Valley fever, RVF, RVFV, chikungunya, CHIK, CHIKV, dengue, DEN, DENV, yellow fever, YF, and YFV. We also reviewed the infectious disease reference, Field’s Virology, several library catalogues, and the Cochrane Library. Two reviewers independently reviewed and categorized abstracts. Abstracts summarizing a study of human infection of one of the six mosquito-borne viruses included in this review were designated for full-text review. The reviewers resolved discrepancies through discussion and consensus. This review satisfies the PRISMA and QUORUM systematic review checklists. Assessment. Assessment was performed on documents included in the full-text review as described in Lessler and others.6 Documents were classified as either containing a statement of the incubation period or not. Those containing an incubation period statement were further classified according to whether the statement was 1) based on and ascertainable from original data, 2) based on but not ascertainable from original data, 3) sourced, or 4) unsourced. Those not containing an incubation period statement were further classified according to whether the article 1) contained original data that could be used to ascertain an incubation period, 2) contained original data that could not be used to ascertain an incubation period, or 3) did not contain any original data. Two reviewers abstracted incubation period statements and original incubation period data as described in Lessler and others.6 We report the incubation period range consistent with over 50% of the abstracted statements. Pooled analysis. As in Lessler and others,6 original data that could be used to ascertain an incubation period were abstracted as doubly interval-censored observations. Assuming a log-normal distribution, incubation period quantiles and a dispersion parameter were estimated for each virus by maximum-likelihood using the coarseDataTools package for R.8 We used 500 bootstrapped samples to calculate 95% confidence intervals (CIs). For each of DENV, WNV, and YFV, pooled data were analyzed 1) including only those who were infected by a mosquito, and 2) including all abstracted cases. For each of CHIKV, JEV, and RVFV, pooled data were analyzed including all abstracted cases, because there were not enough mosquito-infection observations to perform separate analyses. Cases of maternalchild transmission were excluded from the analyses. We INTRODUCTION Mosquito-borne viruses are a major public health threat. Dengue virus (DENV), endemic in tropical settings, has recently spread to more temperate climes, causing an estimated 50–100 million infections and 12,500 deaths per year.1 Similarly, epidemics of West Nile virus (WNV) are a growing concern—a 2012 epidemic in the United States caused 5,674 reported cases (51% of them neuroinvasive) and 286 deaths.2 Knowledge of the incubation period (the time between infection and the onset of symptoms) would improve 1) estimation of the timing, and hence the probable location, of infection;3,4 2) accurate modeling of the disease process using predictive models; and 3) evaluation of control measures (including quarantine) targeting symptomatic individuals.5 However, the incubation periods of many mosquito-borne viruses are typically uncited, nonspecific, and not based on data.6,7 With the previously mentioned gaps in mind, we systematically reviewed the published literature on six mosquito-borne viruses selected for their public health importance: chikungunya virus (CHIKV), DENV, Japanese encephalitis virus (JEV), Rift Valley fever virus (RVFV), WNV, and yellow fever virus (YFV). For each virus, we aim to 1) identify the literature’s consensus on the incubation period, 2) evaluate the evidence for this consensus, and 3) provide estimates of the incubation period that contain detail on the distribution based on published experimental and observational data. MATERIALS AND METHODS Search, assessment, data abstraction, and analyses largely followed the methods of Lessler and others.6 Search strategy and selection criteria. Searches were conducted using PubMed, Google Scholar, and ISI Web of Knowledge 4.0 as described in Lessler and others.6 Searches were conducted between April 15, 2010 and January 6, 2011, with no restrictions on the earliest date of the articles returned. Each search was done with common variations of the virus name, specifically: Japanese encephalitis, Japanese *Address correspondence to Justin Lessler, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 615 N. Wolfe St., E6545, Baltimore, MD 21205. E-mail: 882 883 INCUBATION PERIODS OF MOSQUITO-BORNE VIRAL INFECTIONS Figure 1. Systematic review process. conducted a separate analysis of cases infected by WNV through blood transfusion or surgery. All analyses were done using the R statistical package (version 2.14.1). All data and a complete bibliography are available from the authors upon request. RESULTS We identified 977 articles containing incubation period statements (Figure 1). Table 1 summarizes the incubation periods stated in the literature for each virus. Of the 375 estimates included in these articles, 34 (9%) were original, 129 (34%) were not original but provided a source, and 212 (57%) were not original and did not provide a source. Table 2 summarizes the 60 articles containing individuallevel data appropriate for pooled analysis (Table 2). Estimates for the incubation period of YFV and DENV had the most supp (...truncated)