Factors associated with measles resurgence in the United States in the post-elimination era

Abstract

There have been growing concerns of a potential re-establishment of measles transmission in the United States (US) in the years to come. This study aims to explore potential factors underlying the resurgence of measles in the US by objectively assessing the associations between annual incidence rates (AIR), case importation, vaccination status and disease outbreaks. Data on measles transmission between January 1st, 2001 and December 31st, 2019 were obtained from the national centres for disease control and prevention (CDC) surveillance databases and other published reports. Changes in incidence rates over time were assessed by binomial regression models. Of the 3874 cases of measles in the US over the study period, 3506 (90.5%, 95% CI: 89.5-91.4) occurred in US residents. The AIR per million population in US residents over this period was 0.60 (95% CI: 0.59-0.61), with an overall significant increase over time (p = 0.011). The median percentage of imported and vaccinated cases were 36% [17.9-46.6] and 15% [12.1-23.2] respectively. There was a significant decrease in the percentage of imported cases (p < 0.001) but not of vaccinated cases (p = 0.159) over time. There was a moderate and weak negative correlation between the AIR and the percentage of imported and vaccinated cases respectively (r = -0.59 and r = -0.27 respectively). On multiple linear regression there was a significant linear association between the AIR and the number of outbreaks (p = 0.003) but not with the percentage of imported cases (p = 0.436) and vaccinated cases (p = 0.692), R² = 0.73. Strong negative and positive correlations were seen between the number of outbreaks and the percentage of imported cases (r = -0.61) and the of number states affected (r = 0.88) respectively. Despite the overall reduction in the percentage of imported cases of measles over the past two decades, pockets of internal transmission of the disease following importation via increasing number of outbreaks in unvaccinated subpopulations, reinforced by vaccine hesitancy, account for the sustained increase in measles incidence rates in the US. Controlling indigenous transmission through efficient vaccination coverage in at-risk subpopulations and among international US travellers, improved disease surveillance and rapid outbreak containment are essential in curbing the measles resurgence.

Figure 1

(a) Total annual incidence rate of measles and total number of measles cases between 2001 and 2019. (b) Annual incidence rate of measles and number of measles cases in US residents between 2001 and 2019. The light blue shading represents the number of cases and the connected line represents the annual incidence rate (AIR) per million population. The total AIR and the AIR in US residents was relatively constant between 2001 and 2013, but there were subsequent peaks in 2014 and 2019.

Figure 2

(a) Annual incidence rate of measles in US residents and the percentage of imported cases between 2001 and 2019. (b) Annual incidence rate of measles in US residents and the percentage of vaccinated cases between 2001 and 2019. The red line represents the annual incidence rate (AIR) per million population and the blue connected line represents the percentage of imported cases and vaccinated respectively. Missing data on the percentage of vaccinated US resident cases for 2016 and 2017 in Fig. 2b. There was a decrease in the percentage of imported cases from 46.6% in 2001 to 6.3% in 2019.

Figure 3

(a) Linear regression model of the association between the annual incidence rate and the percentage of imported cases. (b) Linear regression model of the association between the annual incidence rate and the percentage of vaccinated cases. (c) Linear regression model of the association between the number of outbreaks and the percentage of imported cases. (d) Linear regression model of the association between the number of outbreaks and the percentage of unvaccinated cases.

Figure 4

(a) Number of measles outbreaks and number of states affected by measles between 2001 and 2019. The red connected line represents the number of states affected and the blue connected line represents the number of outbreaks. There was a significant increase in the number of outbreaks from 10 in 2001 to 22 in 2019. There was a significant increase in the number of states affected from 16 in 22 in 2001 to 31 in 2019. (b) Linear regression model of the association between the number of outbreaks and the number of states affected.