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Deciphering the Impacts of Vaccination and Immunity on Pertussis Epidemiology in Thailand

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Deciphering the Impacts of Vaccination and Immunity on Pertussis Epidemiology in Thailand Deciphering the impacts of vaccination and immunity on pertussis epidemiology in Thailand Julie C. Blackwooda,b,1, Derek A. T. Cummingsc, Hélène Broutind,e, Sopon Iamsirithawornf, and Pejman Rohania,b,g aDepartment of Ecology and Evolutionary Biology and bCenter for the Study of Complex Systems, University of Michigan, Ann Arbor, MI 48109; cDepartment of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205; dMaladies Infectieuses et Vecteurs Ecologie, Génétique, Evolution et Contrôle, Unité Mixte de Recherche, Centre National de la Recherche Scientifique 5290-IRD 224-UM1-UM2, 34394 Montpellier Cedex 5, France; eDivision of International Epidemiology and Population Study, gFogarty International Center, National Institutes of Health, Bethesda, MD 20892; and fBureau of Epidemiology, Ministry of Public Health, Nonthaburi 11000, Thailand Edited by Roy Curtiss III, Arizona State University, Tempe, AZ, and approved April 16, 2013 (received for review December 3, 2012) Pertussis is a highly infectious respiratory disease that is currently transmission contribution of repeat infections, with vaccination responsible for nearly 300,000 annual deaths worldwide, primarily effectively generating herd immunity. in infants in developing countries. Despite sustained high vaccine To verify our conclusions, we use several empirical metrics to uptake, a resurgence in pertussis incidence has been reported in demonstrate that there is a true increase in herd immunity. We a number of countries. This resurgence has led to critical questions document dramatic changes in patterns of pertussis epidemiol- regarding the transmission impacts of vaccination and pertussis ogy, and quantify shifts in population measures of herd immu- immunology. We analyzed pertussis incidence in Thailand—both nity. We report that over the time span of this study, there was age-stratified and longitudinal aggregate reports—over the past a drastic decline in reported pertussis cases from Thailand, an 30 y. To dissect the contributions of waning pertussis immunity effect that is especially pronounced among infants. Coincident and repeat infections to pertussis epidemiology in Thailand fol- with reduced incidence, we also found a rise in the critical lowing a pronounced increase in vaccine uptake, we used likeli- community size. Overall, these observations are consistent with reduced pertussis circulation in Thailand. hood-based statistical inference methods to evaluate the support Our findings shed light on key hotly debated aspects of per- for multiple competing transmission models. We found that, in tussis epidemiology. First, these results indicate that current contrast to other settings, there is no evidence for pertussis re- pediatric immunization programs in Thailand have successfully surgence in Thailand, with each model examined pointing to a sub- reduced pertussis transmission. Second, there is no empirical stantial rise in herd immunity over the past 30 y. Using a variety of evidence for a resurgence in Thailand, with circulation of Bor- fi fi empirical metrics, we veri ed our ndings by documenting signa- detella pertussis effectively controlled by current vaccines. Finally, tures of changing herd immunity over the study period. Impor- repeat infections appear to play an insignificant role in pertussis tantly, this work leads to the conclusion that repeat infections epidemiology in Thailand. have played little role in shaping pertussis epidemiology in Thailand. Our results are surprisingly emphatic in support of measurable im- Results pact of herd immunity given the uncertainty associated with pertus- Pertussis Data in Thailand. Fig. 1 provides a summary of the data sis epidemiology. from Thailand by displaying pertussis incidence, per capita birth rate, and vaccine uptake estimates in Thailand from 1981 to 2000 ertussis, or whooping cough, was historically considered a (see Materials and Methods for data sources). We split the in- Pserious disease of childhood. Because of the high burden of cidence data into three distinct eras, according to vaccine uptake. morbidity and mortality associated with pertussis (1), routine During the first era (1981–1983), immunization levels were in the vaccination programs were implemented in many developed range 26–46%. The second era (1984–1989) was a transitional countries during the 1940s and 1950s that led, in some instances, period with a rapid rise in uptake from ∼40% in 1984 to 90% in to a 99% reduction in reported incidence (2, 3). The success of 1989. Finally, during the years from 1990 to 2000 (third era), these vaccination programs in reducing pertussis notifications led uptake levels exceeded 90%. Pertussis outbreaks in Thailand fi – to optimism over its potential eradication, a sentiment that has were strongly annual during the rst and second eras (1981 since been replaced by widespread concern following high-pro- 1990; Fig. 1). By the third vaccine era, epidemics were no longer fi < file outbreaks in populations with long-standing immunization, signi cantly annual, incidence was low ( 0.12 per 100,000), and with the United States and Australia arguably experiencing the has remained substantially below 1 per 100,000 since 2001, as largest impacts of these resurgences (4–7). shown by the most recently available incidence estimates from Recent attempts to explain contemporary pertussis epidemi- 2009 and 2010 (18, 19). ology have largely attributed the resurgence to the immunolo- As shown in Fig. 1, over the time span of these data, Thailand gical consequences of vaccination and natural infection. In turn, underwent a demographic transition to lower per capita birth uncertainty surrounding the role of a number of potentially key rates (20) in addition to substantial increases in vaccine uptake. players has been highlighted, including the duration of naturally Epidemiological theory has demonstrated that each of these – covariates can lead to decreased incidence by reducing the rate acquired and vaccine-induced immunity (8 11), limited natural – immune boosting following the introduction of vaccine programs at which the pool of susceptibles is replenished (21 23). Indeed, fi a negative relationship exists between pertussis incidence in (10, 12), loss of vaccine ef cacy resulting from antigenic divergence fi r = − : (13, 14), and, crucially, whether vaccines prevent pertussis trans- Thailand and vaccine uptake (correlation coef cient 0 897, mission or simply reduce the incidence of disease (15–17). To assess the population-level consequences of immunity, we confront high- resolution incidence reports in Thailand with modern techniques Author contributions: J.C.B. and P.R. designed research; J.C.B. performed research; J.C.B. for statistical inference to provide a mechanistic interpretation of analyzed data; and J.C.B., D.A.T.C., H.B., S.I., and P.R. wrote the paper. the transmission impact of vaccination on pertussis immunity in The authors declare no conflict of interest. Thailand. Using a series of competing transmission models, we This article is a PNAS Direct Submission. demonstrate that declines in pertussis incidence coinciding with Freely available online through the PNAS open access option. 1 increases in vaccine uptake between 1984 and 1989 arose following To whom correspondence should be addressed. E-mail: [email protected]. BIOLOGY POPULATION reduction in pertussis circulation. Indeed, the maximum-likelihood This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. estimate associated with each model points to a small or negligible 1073/pnas.1220908110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1220908110 PNAS | June 4, 2013 | vol. 110 | no. 23 | 9595–9600 Downloaded by guest on September 24, 2021 1.4 0.024 100 Low uptake Transition to high uptake High uptake 0.023 90 1.2 0.05 0.022 80 1 0.04 0.03 0.021 70 0.02 0.8 0.02 0.01 60 0 95 96 97 98 99 00 09 10 0.6 0.019 Cases per 100,000 50 Vaccine uptake (%) 0.018 0.4 Annual per capita birthrate 40 0.017 0.2 30 0.016 0 0.015 20 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 00 09 10 Year Fig. 1. Time series of monthly pertussis incidence per 100,000 individuals (black), annual vaccine uptake (red), and the annual per capita birth rate (green)in Thailand. (Inset) Incidence data from 1995–2010 at a finer resolution. The background shading represents three distinct vaccine eras: low vaccine uptake followed by a steep transition to high uptake, which subsequently remains at high levels. P = 0:0158), and a positive association between incidence and which modulates the force of infection, potentially reflecting the birth rate (r = 0:814, P = 0:0273). However, as shown in SI Materials extent of antigenic stimulation following exposure. and Methods, the demographic transition had a limited impact on In models II–IV, we assumed loss of immunity occurs at the the overall pertussis dynamics. same rate for both vaccine- and infection-derived immunity, be- cause although naturally acquired immunity may involve a longer Model Selection. Loss of immunity is a critical and hotly debated time scale than vaccine-induced immunity, the limited time span issue in pertussis epidemiology, and has been argued to play of our data rules out the confident estimation of an additional a considerable role in pertussis with the duration of naturally parameter. Further, given the low severity of repeat infections acquired immunity estimated to be between 7 and 20 y and 4 and relative to primary cases, we assumed that all repeat infections 12 y from vaccine-induced immunity (9). Therefore, statistical go unreported in models III and IV. A schematic representation Materials and Methods SI Materials and inference (details in and of each of the four models is provided in Fig. 2. Methods ,) was used to evaluate the performance of the following We used a formal hypothesis test to compare the relative per- competing transmission models: (I) Lifelong immunity. Baseline formance of models I–IV by estimating the maximum-likelihood model that assumes perfect vaccine-induced and naturally ac- ’ SIR parameters and comparing the associated Akaike s information quired immunity [susceptible/infected/recovered ( ) model].
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