Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease
Streptococcus pneumoniae is an opportunistic pathogen that, while usually carried asymptomatically, can cause severe invasive diseases like meningitis and bacteremic pneumonia. A central goal in S. pneumoniae public health management is to identify which serotypes (immunologically distinct strains)...
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Format: | Article |
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Elsevier
2023-12-01
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Series: | Epidemics |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S1755436523000671 |
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author | Benjamin J. Metcalf Kristofer Wollein Waldetoft Bernard W. Beall Sam P. Brown |
author_facet | Benjamin J. Metcalf Kristofer Wollein Waldetoft Bernard W. Beall Sam P. Brown |
author_sort | Benjamin J. Metcalf |
collection | DOAJ |
description | Streptococcus pneumoniae is an opportunistic pathogen that, while usually carried asymptomatically, can cause severe invasive diseases like meningitis and bacteremic pneumonia. A central goal in S. pneumoniae public health management is to identify which serotypes (immunologically distinct strains) pose the most risk of invasive disease. The most common invasiveness metrics use cross-sectional data (i.e., invasive odds ratios (IOR)), or longitudinal data (i.e., attack rates (AR)). To assess the reliability of these metrics we developed an epidemiological model of carriage and invasive disease. Our mathematical analyses illustrate qualitative failures with the IOR metric (e.g., IOR can decline with increasing invasiveness parameters). Fitting the model to both longitudinal and cross-sectional data, our analysis supports previous work indicating that invasion risk is maximal at or near time of colonization. This pattern of early invasive disease risk leads to substantial (up to 5-fold) biases when estimating underlying differences in invasiveness from IOR metrics, due to the impact of carriage duration on IOR. Together, these results raise serious concerns with the IOR metric as a basis for public health decision-making and lend support for multiple alternate metrics including AR. |
first_indexed | 2024-03-08T22:57:59Z |
format | Article |
id | doaj.art-dacb1dd08b9742848b9b50adb8d89104 |
institution | Directory Open Access Journal |
issn | 1755-4365 |
language | English |
last_indexed | 2024-03-08T22:57:59Z |
publishDate | 2023-12-01 |
publisher | Elsevier |
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series | Epidemics |
spelling | doaj.art-dacb1dd08b9742848b9b50adb8d891042023-12-16T06:06:45ZengElsevierEpidemics1755-43652023-12-0145100731Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of diseaseBenjamin J. Metcalf0Kristofer Wollein Waldetoft1Bernard W. Beall2Sam P. Brown3School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia; Centers for Disease Control and Prevention, Atlanta, Georgia; Corresponding authors at: School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia.School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia; Torsby Hospital, Torsby, SwedenCenters for Disease Control and Prevention, Atlanta, GeorgiaSchool of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia; Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia; Corresponding authors at: School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia.Streptococcus pneumoniae is an opportunistic pathogen that, while usually carried asymptomatically, can cause severe invasive diseases like meningitis and bacteremic pneumonia. A central goal in S. pneumoniae public health management is to identify which serotypes (immunologically distinct strains) pose the most risk of invasive disease. The most common invasiveness metrics use cross-sectional data (i.e., invasive odds ratios (IOR)), or longitudinal data (i.e., attack rates (AR)). To assess the reliability of these metrics we developed an epidemiological model of carriage and invasive disease. Our mathematical analyses illustrate qualitative failures with the IOR metric (e.g., IOR can decline with increasing invasiveness parameters). Fitting the model to both longitudinal and cross-sectional data, our analysis supports previous work indicating that invasion risk is maximal at or near time of colonization. This pattern of early invasive disease risk leads to substantial (up to 5-fold) biases when estimating underlying differences in invasiveness from IOR metrics, due to the impact of carriage duration on IOR. Together, these results raise serious concerns with the IOR metric as a basis for public health decision-making and lend support for multiple alternate metrics including AR.http://www.sciencedirect.com/science/article/pii/S1755436523000671Streptococcus pneumoniaeInvasive diseaseVirulenceCompartmental modelCarriage duration |
spellingShingle | Benjamin J. Metcalf Kristofer Wollein Waldetoft Bernard W. Beall Sam P. Brown Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease Epidemics Streptococcus pneumoniae Invasive disease Virulence Compartmental model Carriage duration |
title | Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease |
title_full | Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease |
title_fullStr | Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease |
title_full_unstemmed | Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease |
title_short | Variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease |
title_sort | variation in pneumococcal invasiveness metrics is driven by serotype carriage duration and initial risk of disease |
topic | Streptococcus pneumoniae Invasive disease Virulence Compartmental model Carriage duration |
url | http://www.sciencedirect.com/science/article/pii/S1755436523000671 |
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