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Evidence for the intermediate disturbance hypothesis and exponential decay in replacement in Streptococcus pneumoniae following use of conjugate vaccines

Paulo, A. Cristina, Sá-Leão, Raquel·2022·Scientific Reports
DOI 10.1038/s41598-022-11279-5PMC PMC9079081
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Abstract

Understanding how pneumococci respond to pneumococcal conjugate vaccines (PCVs) is crucial to predict the impact of upcoming higher-valency vaccines. However, stages in pneumococcal community succession following disturbance are poorly understood as long-time series on carriage are scarce and mostly evaluated at end-point measurements. We used a 20-year cross-sectional dataset of pneumococci carried by Portuguese children, and methods from community ecology, to study community assembly and diversity following use of PCV7 and PCV13. Two successional stages were detected upon introduction of each PCV: one in which non-vaccine serotypes increased in abundance, fitted by a broken-stick model, and a second in which the community returned to the original structure, fitted by a geometric series, but with different serotype profile and a drop in richness as great as 24%. A peak in diversity was observed for levels of intermediate vaccine uptake (30–40%) in agreement with the intermediate disturbance hypothesis. Serotype replacement was fitted by an exponential decay model (R2 = 80%, P < 0.001). The half-life for replacement was 8 years for PCV7 and 10 years for PCV13. The structure of the pneumococcal community is resilient to vaccine pressure. The increasing loss of diversity, however, suggests it could eventually reach a threshold beyond which it may no longer recover.

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Figure 1 Estimates of pneumococcal serotype diversity per sampling year. (a) Richness, 0D; (b) Diversity, 1D (exponential of Shannon’s diversity); (c) Diversity, 2D (inverse of Simpson’s index); (d) Evenness, 1D/0D. For each year a boxplot summarizes the data corresponding to estimates of diversity derived from 1,000 bootstrap re-samplings of 275 children. A smooth line, in red, was imposed to each plot. The differences between the diversity medians are shown as 95% bootstrap confidence intervals. Pneumococcal vaccine uptake is shown at the bottom of the image.
Figure 1 Estimates of pneumococcal serotype diversity per sampling year. (a) Richness, 0D; (b) Diversity, 1D (exponential of Shannon’s diversity); (c) Diversity, 2D (inverse of Simpson’s index); (d) Evenness, 1D/0D. For each year a boxplot summarizes the data corresponding to estimates of diversity derived from 1,000 bootstrap re-samplings of 275 children. A smooth line, in red, was imposed to each plot. The differences between the diversity medians are shown as 95% bootstrap confidence intervals. Pneumococcal vaccine uptake is shown at the bottom of the image.CC BY · PubMed Central
Figure 2 Impact of vaccination on pneumococcal serotype diversity. Partial plots resulting from the fit of a GAM model with three smooth terms to 2D are shown. (a) Changes in 2D according to year; (b) Changes 2D according to smooth term PCV7 uptake; (c) Changes in 2D according to smooth term PCV13 uptake. Smooth functions represent an assembly of polynomials joined together by knots. Each smooth term was significantly associated with 2D (P < 2e-16 for each term).
Figure 2 Impact of vaccination on pneumococcal serotype diversity. Partial plots resulting from the fit of a GAM model with three smooth terms to 2D are shown. (a) Changes in 2D according to year; (b) Changes 2D according to smooth term PCV7 uptake; (c) Changes in 2D according to smooth term PCV13 uptake. Smooth functions represent an assembly of polynomials joined together by knots. Each smooth term was significantly associated with 2D (P < 2e-16 for each term).CC BY · PubMed Central
Figure 3 Pneumococcal serotype succession and community structure. Rank abundance curves depicting relative serotype abundance distribution per year. Each panel shows the serotypes (circles) ranked by the logarithm of their relative abundance. Large black circles indicate serotypes targeted by PCV7, large gray circles indicate the six serotypes targeted by PCV13 only, smaller white circles indicate serotypes not targeted by PCV13. Dashed lines in all panels correspond to 95% confidence interval of serotypes abundance during the pre-PCV period (from 1996 to 2001 as indicated in the first panel). Red lines shows the distribution that better fits the data in each year. Below each year, the name of the distribution that better fits the data is indicated. For the geometric distributions, the slope (k) is also indicated.
Figure 3 Pneumococcal serotype succession and community structure. Rank abundance curves depicting relative serotype abundance distribution per year. Each panel shows the serotypes (circles) ranked by the logarithm of their relative abundance. Large black circles indicate serotypes targeted by PCV7, large gray circles indicate the six serotypes targeted by PCV13 only, smaller white circles indicate serotypes not targeted by PCV13. Dashed lines in all panels correspond to 95% confidence interval of serotypes abundance during the pre-PCV period (from 1996 to 2001 as indicated in the first panel). Red lines shows the distribution that better fits the data in each year. Below each year, the name of the distribution that better fits the data is indicated. For the geometric distributions, the slope (k) is also indicated.CC BY · PubMed Central
Figure 4 Similarity between pneumococcal communities following introduction of PCVs. (a) Bray–Curtis similarity index over time; (b) proportion of the Bray–Curtis similarity index explained by serotype replacement (balanced variation in abundance); (c) proportion of the Bray–Curtis similarity explained by serotype expassion/reduction (gradient component). For the period 2002–2010, when PCV7 was used, the similarity of each year was compared with the pneumococcal serotype community of 2001; for the period 2011–2016, when PCV13 was used, the similarity of each year was compared with the pneumococcal serotype community in 2010. Boxplots represent the summary of 1000 similarity estimates based on bootstrap re-sampling. In (a) and (b), for each period an exponential decay model was fitted to the data: the red solid line corresponds to the PCV7 period, the black solid line corresponds to the PCV13 period. The slope, the significance of the model, and the variance (R2) explained by each model, are indicated.
Figure 4 Similarity between pneumococcal communities following introduction of PCVs. (a) Bray–Curtis similarity index over time; (b) proportion of the Bray–Curtis similarity index explained by serotype replacement (balanced variation in abundance); (c) proportion of the Bray–Curtis similarity explained by serotype expassion/reduction (gradient component). For the period 2002–2010, when PCV7 was used, the similarity of each year was compared with the pneumococcal serotype community of 2001; for the period 2011–2016, when PCV13 was used, the similarity of each year was compared with the pneumococcal serotype community in 2010. Boxplots represent the summary of 1000 similarity estimates based on bootstrap re-sampling. In (a) and (b), for each period an exponential decay model was fitted to the data: the red solid line corresponds to the PCV7 period, the black solid line corresponds to the PCV13 period. The slope, the significance of the model, and the variance (R2) explained by each model, are indicated.CC BY · PubMed Central
Figure 5 Profiles of pneumococcal serotype communities. Dendrogram (left) depicting the hierarchical clustering of the Bray–Curtis similarity indexes of pneumococcal serotype communities in each year. Three clusters were identified and are highlighted in red. Heatmap (right) shows the relative abundance of each serotype. Green numbers close to dendrogram branches indicate bootstrap probability (BP); red numbers close to dendrogram indicate approximately unbiased P (AU); black numbers indicate study years.
Figure 5 Profiles of pneumococcal serotype communities. Dendrogram (left) depicting the hierarchical clustering of the Bray–Curtis similarity indexes of pneumococcal serotype communities in each year. Three clusters were identified and are highlighted in red. Heatmap (right) shows the relative abundance of each serotype. Green numbers close to dendrogram branches indicate bootstrap probability (BP); red numbers close to dendrogram indicate approximately unbiased P (AU); black numbers indicate study years.CC BY · PubMed Central

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Authors
Paulo, A. C., & Sá-Leão, R.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2022-05-07
Volume
12
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-022-11279-5
PMC
PMC9079081
Cited by
6
References
2
Language
en
Licence
Funders
  • Fundação para a Ciência e a Tecnologia,Portugal (SFRH/PBD/99638/2014)
  • Programa Operacional Temático Factores de Competitividade (LISBOA-01-0145-FEDER-007660)

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