Characterizing the epidemiology of the 2009 influenza A/H1N1 pandemic in Mexico

Abstract

Background: Mexico's local and national authorities initiated an intense public health response during the early stages of the 2009 A/H1N1 pandemic. In this study we analyzed the epidemiological patterns of the pandemic during April-December 2009 in Mexico and evaluated the impact of nonmedical interventions, school cycles, and demographic factors on influenza transmission.

Methods and findings: We used influenza surveillance data compiled by the Mexican Institute for Social Security, representing 40% of the population, to study patterns in influenza-like illness (ILIs) hospitalizations, deaths, and case-fatality rate by pandemic wave and geographical region. We also estimated the reproduction number (R) on the basis of the growth rate of daily cases, and used a transmission model to evaluate the effectiveness of mitigation strategies initiated during the spring pandemic wave. A total of 117,626 ILI cases were identified during April-December 2009, of which 30.6% were tested for influenza, and 23.3% were positive for the influenza A/H1N1 pandemic virus. A three-wave pandemic profile was identified, with an initial wave in April-May (Mexico City area), a second wave in June-July (southeastern states), and a geographically widespread third wave in August-December. The median age of laboratory confirmed ILI cases was ∼ 18 years overall and increased to ∼ 31 years during autumn (p<0.0001). The case-fatality ratio among ILI cases was 1.2% overall, and highest (5.5%) among people over 60 years. The regional R estimates were 1.8-2.1, 1.6-1.9, and 1.2-1.3 for the spring, summer, and fall waves, respectively. We estimate that the 18-day period of mandatory school closures and other social distancing measures implemented in the greater Mexico City area was associated with a 29%-37% reduction in influenza transmission in spring 2009. In addition, an increase in R was observed in late May and early June in the southeast states, after mandatory school suspension resumed and before summer vacation started. State-specific fall pandemic waves began 2-5 weeks after school reopened for the fall term, coinciding with an age shift in influenza cases.

Conclusions: We documented three spatially heterogeneous waves of the 2009 A/H1N1 pandemic virus in Mexico, which were characterized by a relatively young age distribution of cases. Our study highlights the importance of school cycles on the transmission dynamics of this pandemic influenza strain and suggests that school closure and other mitigation measures could be useful to mitigate future influenza pandemics. Please see later in the article for the Editors' Summary.

Figure 1. Daily number of laboratory-confirmed A/H1N1 pandemic influenza cases from April 1 to December 31, 2009 in the 32 Mexican states sorted by distance from Mexico City.

For visualization purposes, the time series are log-transformed.

Figure 2. Daily epidemic curve in northern, central, and southeastern states of Mexico, April 1 to December 31, 2009, based on laboratory-confirmed A/H1N1 pandemic influenza cases.

Figure 3. Maps of laboratory-confirmed A/H1N1 pandemic cases across Mexican states for the entire study period, April–December 2009, and by pandemic wave.

The spring wave (April 1–May 20) was focused on the central region, including the state of Mexico, Distrito Federal, Jalisco, Puebla, San Luis Potosi, Guerrero, Hidalgo, and Tlaxcala. The summer wave (May 21–August 1) was concentrated in the southeast states of Veracruz, Yucatan, Quintana Roo, Chiapas, Oaxaca, Tabasco, and Campeche. The fall wave (August 2–December 31) affected the central region and the northern states of Baja California Norte, Sonora, Chihuahua, Coahuila, Nuevo Leon, and Tamaulipas. For each pandemic wave, the color scale range was set according to the highest number of cases across states.

Figure 4. Trends in influenza pandemic patterns and school activities.

(A) H1N1 cases, natural scale; (B) H1N1 cases, log-scale, (C) testing rates (n tests/n ILI), and (D) proportion of hospitalizations among ILI cases during the spring pandemic wave in central Mexico in 2009. Shaded areas denote periods when schools are not in session, including during the spring break (April 4–18) and the mandatory suspension of educational activities (April 24–May 11). (B) indicates changes in the R estimates over time, as measured from the exponential growth rate of the incidence curves.

Figure 5. Fit of influenza transmission model to the daily number of H1N1 pandemic influenza cases in central Mexico, April 1–May 11, 2009.

The grey shaded area indicates the suspension of educational activities and other social distancing measures implemented between April 24 and May 11, 2009. Black circles represent the observed data. The solid red line is the model best-fit, and the blue lines are CIs based on 100 realizations of the model obtained by parametric bootstrapping (Text S1).

Figure 6. Changes in the age distribution of cases during the summer and fall pandemic waves in Mexico.

(A) Weekly time series of laboratory-confirmed A/H1N1 pandemic cases among students (5–20 y, red curve) and other age groups (blue curve) and (B) Weekly ratio of student to nonstudent A/H1N1 cases. The grey shaded area indicates the mandatory school closure period (April 24–May 11) and the summer vacation period (July 3–August 23) for elementary and secondary school students. College students retuned to class on August 10th(arrow).