Changes in the incidence of invasive disease due to Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis during the COVID-19 pandemic in 26 countries and territories in the Invasive Respiratory Infection Surveillance Initiative: a prospective analysis of surveillance data

Angela B. Brueggemann, Melissa J. Jansen van Rensburg, David Shaw, Noel D. McCarthy, Keith A. Jolley, Martin C.J. Maiden, Mark P.G. van der Linden, Zahin Amin-Chowdhury, Désirée E. Bennett, Raymond Borrow, Maria Cristina C. Brandileone, Karen Broughton, Ruth Campbell, Bin Cao, Carlo Casanova, Eun Hwa Choi, Yiu Wai Chu, Stephen Clark, Heike Claus, Juliana CoelhoMary Corcoran, Simon Cottrell, Robert J. Cunney, Tine Dalby, Heather Davies, Linda de Gouveia, Ala Eddine Deghmane, Walter Demczuk, Stefanie Desmet, Richard J. Drew, Mignon du Plessis, Helga Erlendsdottir, Norman Fry, Kurt Fuursted, Steve J. Gray, Birgitta Henriques-Normark, Thomas Hale, Markus Hilty, Steen Hoffmann, Hilary Humphreys, Margaret Ip, Susanne Jacobsson, Jillian Johnston, Jana Kozakova, Karl G. Kristinsson, Pavla Krizova, Alicja Kuch, Shamez Ladhani, Thiên Trí Lâm, Vera Lebedova, Laura Lindholm, David Litt, Irene Martin, Delphine Martiny, Wesley Mattheus, Martha McElligott, Mary Meehan, Susan Meiring, Paula Mölling, Eva Morfeldt, Julie Morgan, Robert M. Mulhall, Carmen Muñoz-Almagro, David R. Murdoch, Joy Murphy, Martin Musilek, Alexandre Mzabi, Amaresh Perez-Argüello, Monique Perrin, Malorie Perry, Alba Redin, Richard Roberts, Maria Roberts, Assaf Rokney, Merav Ron, Kevin J. Scott, Carmen Clark, Lotta Siira, Anna Skoczyńska, Monica Sloan, Hans Christian Slotved, Andrew J. Smith, Joon Young Song, Muhamed Kheir Taha, Maija Toropainen, Dominic Tsang, Anni Vainio, Nina M. van Sorge, Emmanuelle Varon, Jiri Vlach, Ulrich Vogel, Sandra Vohrnova, Anne von Gottberg, Rosemeire C. Zanella, Fei Zhou

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Abstract

BACKGROUND: Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis, which are typically transmitted via respiratory droplets, are leading causes of invasive diseases, including bacteraemic pneumonia and meningitis, and of secondary infections subsequent to post-viral respiratory disease. The aim of this study was to investigate the incidence of invasive disease due to these pathogens during the early months of the COVID-19 pandemic. 

METHODS: In this prospective analysis of surveillance data, laboratories in 26 countries and territories across six continents submitted data on cases of invasive disease due to S pneumoniae, H influenzae, and N meningitidis from Jan 1, 2018, to May, 31, 2020, as part of the Invasive Respiratory Infection Surveillance (IRIS) Initiative. Numbers of weekly cases in 2020 were compared with corresponding data for 2018 and 2019. Data for invasive disease due to Streptococcus agalactiae, a non-respiratory pathogen, were collected from nine laboratories for comparison. The stringency of COVID-19 containment measures was quantified using the Oxford COVID-19 Government Response Tracker. Changes in population movements were assessed using Google COVID-19 Community Mobility Reports. Interrupted time-series modelling quantified changes in the incidence of invasive disease due to S pneumoniae, H influenzae, and N meningitidis in 2020 relative to when containment measures were imposed. 

FINDINGS: 27 laboratories from 26 countries and territories submitted data to the IRIS Initiative for S pneumoniae (62 837 total cases), 24 laboratories from 24 countries submitted data for H influenzae (7796 total cases), and 21 laboratories from 21 countries submitted data for N meningitidis (5877 total cases). All countries and territories had experienced a significant and sustained reduction in invasive diseases due to S pneumoniae, H influenzae, and N meningitidis in early 2020 (Jan 1 to May 31, 2020), coinciding with the introduction of COVID-19 containment measures in each country. By contrast, no significant changes in the incidence of invasive S agalactiae infections were observed. Similar trends were observed across most countries and territories despite differing stringency in COVID-19 control policies. The incidence of reported S pneumoniae infections decreased by 68% at 4 weeks (incidence rate ratio 0·32 [95% CI 0·27-0·37]) and 82% at 8 weeks (0·18 [0·14-0·23]) following the week in which significant changes in population movements were recorded. 

INTERPRETATION: The introduction of COVID-19 containment policies and public information campaigns likely reduced transmission of S pneumoniae, H influenzae, and N meningitidis, leading to a significant reduction in life-threatening invasive diseases in many countries worldwide. FUNDING: Wellcome Trust (UK), Robert Koch Institute (Germany), Federal Ministry of Health (Germany), Pfizer, Merck, Health Protection Surveillance Centre (Ireland), SpID-Net project (Ireland), European Centre for Disease Prevention and Control (European Union), Horizon 2020 (European Commission), Ministry of Health (Poland), National Programme of Antibiotic Protection (Poland), Ministry of Science and Higher Education (Poland), Agencia de Salut Pública de Catalunya (Spain), Sant Joan de Deu Foundation (Spain), Knut and Alice Wallenberg Foundation (Sweden), Swedish Research Council (Sweden), Region Stockholm (Sweden), Federal Office of Public Health of Switzerland (Switzerland), and French Public Health Agency (France).

Original languageEnglish
Pages (from-to)e360-e370
JournalThe Lancet Digital Health
Volume3
Issue number6
Early online date24 May 2021
DOIs
Publication statusPublished - 1 Jun 2021

Bibliographical note

Funding Information: The following authors received support for work unrelated to this study: MPGvdL has received grants from Pfizer, Merck, and the Robert Koch Institut; RB has done contract research on behalf of Public Health England for GlaxoSmithKline, Pfizer, and Sanofi Pasteur, but received no personal remuneration; MC has received grants from Pfizer; SAC has done contract research on behalf of Public Health England for GlaxoSmithKline, Pfizer, and Sanofi Pasteur, but received no personal remuneration; SD has received a grant from Pfizer; SJG did contract research (carriage studies) for vaccine manufacturers (GlaxoSmithKline and Pfizer) on behalf of Public Health England, but received no personal remuneration; MH has received grants from Pfizer and the Federal Office of Public Health, and personal fees (for being on an advisory board) from Pfizer and Merck Sharp & Dohme; HH has received grants from Astellas and Pfizer; KAJ has received a grant from Wellcome Trust and personal fees from GlaxoSmithKline; SNL has done contract research for vaccine manufacturers (GlaxoSmithKline, Pfizer, and Sanofi Pasteur) on behalf of St. George's University of London, but received no personal remuneration; DJL has received grants from GlaxoSmithKline and Pfizer; SM has received a grant from Sanofi Pasteur; CM-A has received grants from Quiastat, Roche, Pfizer, and Genomica, and personal fees from Roche, Pfizer, and Qiagen; LS has received a grant from GlaxoSmithKline; H-CS has received a grant from Pfizer; MI has received non-financial support from GlaxoSmithKline and Pfizer, personal fees from Pfizer (speaker fees) and Merck Sharp & Dohme (speaker fees), and grants from Merck Sharp & Dohme; M-KT has received grants from GlaxoSmithKline, Pfizer, and Sanofi Pasteur; ASk has received grants and non-financial support from Pfizer, and personal fees from Pfizer, Merck Sharp & Dohme, and Sanofi Pasteur; CLS has received grants from Pfizer and GlaxoSmithKline for investigator-led research; EV has received grants on behalf of her institution (Intercommunal Hospital of Créteil) from Pfizer and Merck Sharp & Dohme; MT has received grants from GlaxoSmithKline and Pfizer; NKF's institution (Public Health England) has received funding for investigator-initiated research from GlaxoSmithKline, Pfizer, and Affinivax, but NKF received no personal remuneration; AvG has received a grant from Sanofi Pasteur; NMvS has received a grant from Pfizer, a fee for service paid to their institution from Merck Sharp & Dohme and GlaxoSmithKline, and also has a patent (WO 2013/020090 A3) on vaccine development against Streptococcus pyogenes, unrelated to this study, with royalties paid to University of California San Diego, CA, USA; and MKT has a patent (630133) for a vaccine for serogroup X meningococcus with GlaxoSmithKline. All other authors declare no competing interests.
We thank all the hospitals and clinical microbiology laboratories who submitted data and isolates to the reference laboratories as part of their surveillance programmes. We acknowledge the assistance of laboratory personnel who made important contributions to the microbiological data in this study: Wendy Keijzers, Ilse Schuurman, and Agaath Arends in the Netherlands Reference Laboratory for Bacterial Meningitis, Amsterdam, The Netherlands; Marie-Cécile Ploy, Carole Grelaud, and all the microbiologists of the French Regional Observatory of Pneumococci Network (Limoges, France); Alice Enefer, Anna Lewis, Karina Micah, Samuel Rose, Chenchal Dhami, and Roger Daniel at the Public Health England Respiratory and Vaccine Preventable Bacteria Unit, London, UK; Xilian Bai, Aiswarya Lekshmi, Jay Lucidarme, Andrew Walker, Lloyd Walsh, and Laura Willerton at the Public Health England Meningococcal Reference Unit in Manchester, UK; Ana Paula Silva de Lemos and Samanta Cristine Grassi Almeida at the National Laboratory for Meningitis and Pneumococcal Infections, São Paulo, Brazil; and the technicians from the Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark. The infrastructure for the IRIS Initiative was funded by a Wellcome Trust Investigator Award to ABB (grant number 206394/Z/17/Z) and a Wellcome Trust Biomedical Resource Grant to MJCM, ABB, and KAJ (grant number 218205/Z/19/Z). The German National Reference Center for Streptococci receives financial support from the Robert Koch Institute with funds from the Federal Ministry of Health (funding code 1369-235), Pfizer, and Merck. The German National Reference Laboratory for Meningococci and Haemophilus influenzae is supported by the Robert Koch Institute with funds from the Federal Ministry of Health (funding code 1369-237). The Irish Meningitis and Sepsis Reference Laboratory has received support from Children's Health Ireland at Temple Street, Royal College of Surgeons, Health Protection Surveillance Centre, and the SpID-Net project, which has received funding from the European Centre for Disease Prevention and Control and Horizon 2020. Children's Health Ireland at Temple Street has previously received research funds from Pfizer to partially support this work. The Polish data collection was partially supported by the Ministry of Health within the framework of the National Programme of Antibiotic Protection, by the Ministry of Science and Higher Education (Mikrobank 2 Programme), and by a research grant from Pfizer. Funding for materials, equipment, and human resources associated with the laboratory in Catalonia (Spain) was provided by Agencia de Salut Pública de Catalunya and Sant Joan de Deu Foundation. BH-N received funding from the Knut and Alice Wallenberg Foundation, the Swedish Research Council, and Region Stockholm. The Swiss National Reference Centre for Invasive Pneumococci is funded by the Federal Office of Public Health of Switzerland. The National Reference Centre for Pneumococci in Créteil (France) received funding from the French Public Health Agency.

Open Access: This is an Open Access article under the CC BY 4.0 license.

Publisher Copyright: © 2021 The Author(s). Published by Elsevier Ltd.

Citation: Brueggemann, Angela B., et al. "Changes in the incidence of invasive disease due to Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis during the COVID-19 pandemic in 26 countries and territories in the Invasive Respiratory Infection Surveillance Initiative: a prospective analysis of surveillance data." The Lancet Digital Health 3.6 (2021): e360-e370.

DOI: https://doi.org/10.1016/S2589-7500(21)00077-7

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