Emergence of pertactin-deficient pertussis strains in Australia can be explained by models of vaccine escape

Jayasundara, Duleepa; Lee, Edward; Octavia, Sophie; Lan, Ruiting; Tanaka, Mark M.; Wood, James G.

doi:10.1016/j.epidem.2020.100388

Cited by 11 publications

(10 citation statements)

References 26 publications

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“…Various potential explanations have been offered in the literature for the recent re-emergence of pertussis in highly vaccinated populations such as England and Wales, including changes in the vaccine schedule and diagnostics [ 32 ], vaccine failure [ 36 , 37 , 83 – 87 ], waning of vaccine immunity [ 37 , 85 , 88 – 90 ], differences in the efficacy of acellular and whole cell vaccines [ 36 , 37 , 86 ], changes in the population contact structure [ 36 , 45 ], the impact of asymptomatic transmission [ 89 , 91 – 94 ] perhaps associated with the introduction of acellular vaccines [ 37 , 77 ], and failure in the degree of vaccine protection [ 32 , 83 , 95 ], possibly arising from vaccine-driven evolution [ 96 , 97 ]. In addition, it is worth pointing out that there was a notable decreasing trend in the vaccine coverage rates across the boroughs of London in the years preceding the 2012 epidemic ( Fig 1A ), whose potential role in the re-emergence of pertussis requires further systematic investigation.…”

Section: Discussionmentioning

confidence: 99%

Dissecting recurrent waves of pertussis across the boroughs of London

2022

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Pertussis has resurfaced in the UK, with incidence levels not seen since the 1980s. While the fundamental causes of this resurgence remain the subject of much conjecture, the study of historical patterns of pathogen diffusion can be illuminating. Here, we examined time series of pertussis incidence in the boroughs of Greater London from 1982 to 2013 to document the spatial epidemiology of this bacterial infection and to identify the potential drivers of its percolation. The incidence of pertussis over this period is characterized by 3 distinct stages: a period exhibiting declining trends with 4-year inter-epidemic cycles from 1982 to 1994, followed by a deep trough until 2006 and the subsequent resurgence. We observed systematic temporal trends in the age distribution of cases and the fade-out profile of pertussis coincident with increasing national vaccine coverage from 1982 to 1990. To quantify the hierarchy of epidemic phases across the boroughs of London, we used the Hilbert transform. We report a consistent pattern of spatial organization from 1982 to the early 1990s, with some boroughs consistently leading epidemic waves and others routinely lagging. To determine the potential drivers of these geographic patterns, a comprehensive parallel database of borough-specific features was compiled, comprising of demographic, movement and socio-economic factors that were used in statistical analyses to predict epidemic phase relationships among boroughs. Specifically, we used a combination of a feed-forward neural network (FFNN), and SHapley Additive exPlanations (SHAP) values to quantify the contribution of each covariate to model predictions. Our analyses identified a number of predictors of a borough’s historical epidemic phase, specifically the age composition of households, the number of agricultural and skilled manual workers, latitude, the population of public transport commuters and high-occupancy households. Univariate regression analysis of the 2012 epidemic identified the ratio of cumulative unvaccinated children to the total population and population of Pakistan-born population to have moderate positive and negative association, respectively, with the timing of epidemic. In addition to providing a comprehensive overview of contemporary pertussis transmission in a large metropolitan population, this study has identified the characteristics that determine the spatial spread of this bacterium across the boroughs of London.

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Section: Discussionmentioning

confidence: 99%

Dissecting recurrent waves of pertussis across the boroughs of London

2022

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“…They were also shown to be almost as pathogenic in infants [ 34 , 48 , 49 ]. It has been hypothesized that the increase of the prevalence of PRN(−) isolates might decrease the aPV efficacy [ 45 , 50 ]. The model developed by Jayasundara et al [ 50 ] suggests that the emergence of PRN(−) strains in the recent epidemics in Australia is vaccine-driven and is the cause of the increase in the incidence of the disease.…”

Section: Discussionmentioning

confidence: 99%

“…It has been hypothesized that the increase of the prevalence of PRN(−) isolates might decrease the aPV efficacy [ 45 , 50 ]. The model developed by Jayasundara et al [ 50 ] suggests that the emergence of PRN(−) strains in the recent epidemics in Australia is vaccine-driven and is the cause of the increase in the incidence of the disease. However, the decrease in disease severity among vaccinated individuals is still apparent [ 48 ] and vaccination against pertussis remains an important public health measure since aPV effectiveness did not seem to be reduced in the context of high prevalence of PRN(−) strains in the USA [ 51 ].…”

Section: Discussionmentioning

confidence: 99%

Can vaccines control bacterial virulence and pathogenicity? Bordetella pertussis: the advantage of fitness over virulence

Guiso

Soubeyrand²,

Macina

2022

Evolution, Medicine, and Public Health

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Some vaccines, such as diphtheria toxoid and acellular pertussis vaccines (aPVs), may favor the emergence of less pathogenic strains of the respective bacteria they target. This review discusses the impact of the wide use of aPV on Bordetella pertussis phenotype evolutions and their beneficial consequences in the light of the diphtheria toxoid immunization program experience and structuring evidence review in a causal analysis following Bradford Hill’s causality criteria. All aPVs contain the pertussis toxin (PT), the main virulence factor of B. pertussis, alone or with one adhesin (Filamentous hemagglutinin (FHA)), two adhesins (FHA and pertactin (PRN)) or four adhesins (FHA, PRN and two fimbriae (Fim 2/3)). In countries where the coverage of aPVs containing PRN is high, PRN negative B. pertussis isolates are increasing in prevalence, but isolates non-producing the other antigens are rarely reported. We hypothesize that the selective pressure at play with PRN should exist against all aVP antigens, although detection biases may hinder its detection for other antigens, especially PT. PT being responsible for clinically frank cases of the disease, the opportunity to collect PT negative isolates is far lower than to collect PRN negative isolates which have a limited clinical impact. The replacement of current B. pertussis by far less pathogenic isolates no longer producing the factors contained in aPVs should be expected as a consequence of the wide aPV use. LAY SUMMARY Reviewing the existing evidence, we hypothesize that acellular whooping cough vaccines induced selective pressure on the bacteria causing whooping cough. To survive the bacteria must stop the production of virulence factors targeted by the vaccine that should decrease the severity of the disease and jeopardise the detection of the bacteria.

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“…Nevertheless, adaptive changes of B. pertussis to aPV pressure may increase waning immunity. Of potential concern, an increase in fitness of vaccine-escape strains may lead to a rapid rise in the proportion of cases due to these strains and an overall increase in pertussis case numbers over a 20-year period [ 270 ].…”

Section: Subversion Of Anti- B Pertussis Immunitymentioning

confidence: 99%

Pathogenicity and virulence of Bordetella pertussis and its adaptation to its strictly human host

et al. 2021

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The highly contagious whooping cough agent Bordetella pertussis has evolved as a human-restricted pathogen from a progenitor which also gave rise to Bordetella parapertussis and Bordetella bronchiseptica . While the latter colonizes a broad range of mammals and is able to survive in the environment, B. pertussis has lost its ability to survive outside its host through massive genome decay. Instead, it has become a highly successful human pathogen by the acquisition of tightly regulated virulence factors and evolutionary adaptation of its metabolism to its particular niche. By the deployment of an arsenal of highly sophisticated virulence factors it overcomes many of the innate immune defenses. It also interferes with vaccine-induced adaptive immunity by various mechanisms. Here, we review data from in vitro , human and animal models to illustrate the mechanisms of adaptation to the human respiratory tract and provide evidence of ongoing evolutionary adaptation as a highly successful human pathogen.

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Emergence of pertactin-deficient pertussis strains in Australia can be explained by models of vaccine escape

Cited by 11 publications

References 26 publications

Dissecting recurrent waves of pertussis across the boroughs of London

Dissecting recurrent waves of pertussis across the boroughs of London

Can vaccines control bacterial virulence and pathogenicity? Bordetella pertussis: the advantage of fitness over virulence

Pathogenicity and virulence of Bordetella pertussis and its adaptation to its strictly human host

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