From the Cover: The role of older children and adults in wild poliovirus transmission

As polio eradication inches closer, the absence of poliovirus circulation in most of the world and imperfect vaccination coverage are resulting in immunity gaps and polio outbreaks affecting adults. Furthermore, imperfect, waning intestinal immunity among older children and adults permits reinfection and poliovirus shedding, prompting calls to extend the age range of vaccination campaigns even in the absence of cases in these age groups. The success of such a strategy depends on the contribution to poliovirus transmission by older ages, which has not previously been estimated. We fit a mathematical model of poliovirus transmission to time series data from two large outbreaks that affected adults (Tajikistan 2010, Republic of Congo 2010) using maximum-likelihood estimation based on iterated particle-filtering methods. In Tajikistan, the contribution of unvaccinated older children and adults to transmission was minimal despite a significant number of cases in these age groups [reproduction number, R = 0.46 (95% confidence interval, 0.42–0.52) for >5-y-olds compared to 2.18 (2.06–2.45) for 0- to 5-y-olds]. In contrast, in the Republic of Congo, the contribution of older children and adults was significant [R = 1.85 (1.83–4.00)], perhaps reflecting sanitary and socioeconomic variables favoring efficient virus transmission. In neither setting was there evidence for a significant role of imperfect intestinal immunity in the transmission of poliovirus. Bringing the immunization response to the Tajikistan outbreak forward by 2 wk would have prevented an additional 130 cases (21%), highlighting the importance of early outbreak detection and response.The Global Polio Eradication Initiative (GPEI) has achieved >99% reduction in the global annual incidence of poliomyelitis since the program began in 1988, and in 2012, just three countries were yet to interrupt wild poliovirus transmission—Afghanistan, Pakistan, and Nigeria—and 223 poliomyelitis cases were reported, the lowest in history (1). However, the absence of wild poliovirus transmission from most of the world, together with long-standing suboptimal vaccination coverage, has created cohorts of susceptible children and adults. As a result, an increased number of polio outbreaks affecting older children and adults have occurred in countries previously free of wild poliovirus (2–6). These outbreaks have significantly raised the cost of the GPEI and are a major challenge to achieving the goal of stopping all transmission by end-2014.It has also become clear that intestinal immunity to poliovirus wanes over time, allowing individuals vaccinated with oral poliovirus vaccine (OPV) to become reinfected and shed poliovirus (7). Therefore, older children and adults could theoretically contribute to wild poliovirus transmission without developing poliomyelitis. The World Health Organization (WHO) has recommended vaccination of older age groups as a standard for outbreak response (8). In addition, the recent GPEI strategic plan proposes expanding the age range of mass vaccination campaigns that currently target 0- to 4-y-old children in endemic countries as a potential measure to accelerate eradication, even though poliomyelitis is rarely reported at older ages (9, 10).Poliovirus shedding may not necessarily result in secondary infections, which depends on where the virus is deposited, routes of transmission, contact rates, and population immunity. Older children and adults are considered more hygienic than younger children, and these behavioral factors may limit onward transmission of shed poliovirus (11). Furthermore, the quantity and duration of virus shedding following reinfection of OPV-vaccinated individuals is reduced compared with naïve individuals (7). Where cases of poliomyelitis among older children and adults are rare, consideration of mass vaccination of this age group therefore requires an understanding of their contribution to transmission. This is challenging, however, because traditional methods such as contact tracing are not possible for wild poliovirus, which causes poliomyelitis in only 1 in ∼200 primary infections (12).In 2010, a large outbreak of imported wild poliovirus type 1 of Indian origin in Tajikistan resulted in 518 cases of poliomyelitis (Fig. 1 A and B) (2). Although this outbreak was associated with poliomyelitis among older children and adults, the initial response with serotype 1 monovalent OPV (mOPV1) targeted children 0–5 y of age, permitting a direct assessment of the contribution of these children and older age groups to transmission. We examined the transmission dynamics during this epidemic and the impact of vaccination by fitting an age-structured mathematical model of transmission using maximum likelihood with a particle-filtering algorithm (13, 14). As a comparison, we also examined the transmission dynamics during a large type 1 poliovirus outbreak in the Republic of Congo that commenced in late 2010 (442 cases of poliomyelitis) (Fig. 2 A and B) following introduction of virus from Angola (3, 15), as this lower income country, with a poorer level of sanitation, is likely to have had a different transmission pattern.Open in a separate windowFig. 1.The 2010 poliomyelitis outbreak in Tajikistan. (A) Geographic distribution of poliomyelitis cases plotted by district and colored according to their age group. The total population size for each district is indicated by the shading. Within a district, dots are randomly placed. (B) The age distribution of reported poliomyelitis cases by week of onset of paralysis. (C) Number of cases of poliomyelitis by week of onset of paralysis by age group (bars) with the median (blue line) and interquartile range (blue shading) of simulations under the best-fit transmission model, conditional on a major epidemic. The median (orange line) and interquartile range (orange shading) for simulations in the absence of a vaccination response are also shown. (D) Predicted number of cases prevented by the age-targeted vaccination response and under alternative scenarios (bars, median; error bars, interquartile range).Open in a separate windowFig. 2.The 2010–2011 poliomyelitis outbreak in the Republic of Congo. (A) Geographic distribution of poliomyelitis cases plotted by district and colored according to their age group. The total population size for each district is indicated by the shading. Within a district, dots are randomly placed. (B) The age distribution of reported poliomyelitis cases by week of onset of paralysis. (C) Number of cases of poliomyelitis by week of onset of paralysis for each age group (bars) with the median (blue line) and interquartile range (blue shading) of simulations under the best-fit transmission model, conditional on a major epidemic. The expected outbreak dynamics in the absence of a response are not shown (compare with Fig. 1) because of uncertainty in the estimated vaccine efficacy.