{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T04:31:49Z","timestamp":1791952309904,"version":"4.3.4"},"reference-count":26,"publisher":"Oxford University Press (OUP)","issue":"10","license":[{"start":{"date-parts":[[2021,8,14]],"date-time":"2021-08-14T00:00:00Z","timestamp":1628899200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,5,30]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Invasive meningococcal disease (IMD) is a devastating illness with high mortality rates. Like influenza, endemic IMD is seasonal, peaking in winter. Studies suggest that circulation of influenza virus may influence the timing and magnitude of IMD winter peaks.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>This ecological study used weekly data from 2 nationwide surveillance programs: Viral Watch (proportion of outpatient influenza-positive cases from throat or nasal swab samples) and GERMS-SA (laboratory-confirmed cases of IMD), occurring across South Africa from 2003 through 2018 in all age bands. A bivariate time series analysis using wavelet transform was conducted to determine cocirculation of the diseases and the time lag between the peak seasons. We modeled excess meningococcal disease cases attributable to influenza cocirculation, using univariate regression spline models. Stata and R statistical software packages were used for the analysis.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>A total of 5256 laboratory-confirmed IMD cases were reported, with an average annual incidence of 0.23 episodes per 100 000 population and a mean seasonal peak during week 32 (\u00b13 weeks). Forty-two percent of swab samples (10 421 of 24 741) were positive for influenza during the study period. The mean peak for all influenza occurred at week 26 (\u00b14 weeks). There was an average lag time of 5 weeks between annual influenza and IMD seasons. Overall, 5% (1%\u20139%) of IMD cases can be attributable to influenza cocirculation, with, on average, 17 excess IMD cases per year attributable to influenza.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>A quantifiable proportion of IMD in South Africa is associated with influenza cocirculation; therefore, seasonal influenza vaccination may have an effect on preventing a small portion of IMD in addition to preventing influenza.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/cid\/ciab702","type":"journal-article","created":{"date-parts":[[2021,8,12]],"date-time":"2021-08-12T11:21:25Z","timestamp":1628767285000},"page":"1729-1735","source":"Crossref","is-referenced-by-count":3,"title":["Excess Invasive Meningococcal Disease Associated With Seasonal Influenza, South Africa, 2003\u20132018"],"prefix":"10.1093","volume":"74","author":[{"given":"Susan","family":"Meiring","sequence":"first","affiliation":[{"name":"Division of Public Health Surveillance and Response, National Institute for Communicable Diseases, a Division of the National Health Laboratory Service , Johannesburg , South Africa"},{"name":"School of Public Health, University of the Witwatersrand , Johannesburg , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefano","family":"Tempia","sequence":"additional","affiliation":[{"name":"School of Public Health, University of the Witwatersrand , Johannesburg , South Africa"},{"name":"Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, a Division of the National Health Laboratory Service , Johannesburg , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emanuel M","family":"Dominic","sequence":"additional","affiliation":[{"name":"South African DSI-NRF Centre of Excellence in Epidemiological Modelling and Analysis (SACEMA), Stellenbosch University , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda","family":"de Gouveia","sequence":"additional","affiliation":[{"name":"Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, a Division of the National Health Laboratory Service , Johannesburg , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jo","family":"McAnerney","sequence":"additional","affiliation":[{"name":"Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, a Division of the National Health Laboratory Service , Johannesburg , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne","family":"von Gottberg","sequence":"additional","affiliation":[{"name":"Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, a Division of the National Health Laboratory Service , Johannesburg , South Africa"},{"name":"School of Pathology, University of the Witwatersrand , Johannesburg , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheryl","family":"Cohen","sequence":"additional","affiliation":[{"name":"School of Public Health, University of the Witwatersrand , Johannesburg , South Africa"},{"name":"Centre for Respiratory Diseases and Meningitis, National Institute for Communicable Diseases, a Division of the National Health Laboratory Service , Johannesburg , South Africa"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,8,14]]},"reference":[{"key":"2022053122502073200_CIT0001","doi-asserted-by":"crossref","first-page":"e107486","DOI":"10.1371\/journal.pone.0107486","article-title":"The association of meningococcal disease with influenza in the United States, 1989\u20132009","volume":"9","author":"Jacobs","year":"2014","journal-title":"PLoS One"},{"key":"2022053122502073200_CIT0002","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1017\/S0950268807000271","article-title":"Invasive pneumococcal and meningococcal disease: association with influenza virus and respiratory syncytial virus activity?","volume":"136","author":"Jansen","year":"2008","journal-title":"Epidemiol Infect"},{"key":"2022053122502073200_CIT0003","doi-asserted-by":"crossref","first-page":"e0128580","DOI":"10.1371\/journal.pone.0128580","article-title":"Potential impact of co-infections and co-morbidities prevalent in Africa on influenza severity and frequency: a systematic review","volume":"10","author":"Cohen","year":"2015","journal-title":"PLoS One"},{"key":"2022053122502073200_CIT0004","doi-asserted-by":"crossref","first-page":"e15493","DOI":"10.1371\/journal.pone.0015493","article-title":"Respiratory virus infection and risk of invasive meningococcal disease in central Ontario, Canada","volume":"5","author":"Tuite","year":"2010","journal-title":"PLoS One"},{"key":"2022053122502073200_CIT0005","volume-title":"Guidelines for the management, prevention and control of meningococcal disease in South Africa","author":"Department of Health.","year":"2011"},{"key":"2022053122502073200_CIT0006","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1093\/cid\/ciy914","article-title":"Declining incidence of invasive meningococcal disease in South Africa: 2003\u20132016","volume":"69","author":"Meiring","year":"2019","journal-title":"Clin Infect Dis"},{"key":"2022053122502073200_CIT0007","first-page":"82","article-title":"Recommendations for the use of meningococcal vaccines in South Africa","volume":"32","author":"Meiring","year":"2017","journal-title":"South African J Infect Dis"},{"key":"2022053122502073200_CIT0008","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1056\/NEJM197207062870102","article-title":"A simultaneous outbreak of meningococcal and influenza infections","volume":"287","author":"Young","year":"1972","journal-title":"N Engl J Med"},{"key":"2022053122502073200_CIT0009","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1016\/0140-6736(91)91112-8","article-title":"Influenza A and meningococcal disease","volume":"338","author":"Cartwright","year":"1991","journal-title":"Lancet"},{"key":"2022053122502073200_CIT0010","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1001\/archinte.1991.00400050141028","article-title":"A cluster of meningococcal disease on a school bus following epidemic influenza","volume":"151","author":"Harrison","year":"1991","journal-title":"Arch Intern Med"},{"key":"2022053122502073200_CIT0011","doi-asserted-by":"crossref","first-page":"e48","DOI":"10.1086\/322609","article-title":"Outbreak of meningococcal disease after an influenza B epidemic at a Hellenic Air Force recruit training center","volume":"33","author":"Makras","year":"2001","journal-title":"Clin Infect Dis"},{"key":"2022053122502073200_CIT0012","volume-title":"Midyear population estimate 2019","author":"Statistics South Africa.","year":"2019"},{"key":"2022053122502073200_CIT0013","volume-title":"GERMS-SA annual report 2018","author":"National Institute for Communicable Diseases.","year":"2019"},{"key":"2022053122502073200_CIT0014","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1093\/infdis\/jis575","article-title":"Twenty-five years of outpatient influenza surveillance in South Africa, 1984\u20132008","volume":"206","author":"McAnerney","year":"2012","journal-title":"J Infect Dis"},{"key":"2022053122502073200_CIT0015","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1093\/cid\/cix740","article-title":"In- and out-of-hospital mortality associated with seasonal and pandemic influenza and respiratory syncytial virus in South Africa, 2009-2013","volume":"66","author":"Cohen","year":"2018","journal-title":"Clin Infect Dis"},{"key":"2022053122502073200_CIT0016","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0064734","volume-title":"Mortality attributable to seasonal and pandemic influenza, Australia, 2003 to 2009, using a novel time series smoothing approach.","author":"Muscatello","year":"2013"},{"key":"2022053122502073200_CIT0017","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1177\/1536867X0700700103","article-title":"Multivariate modeling with cubic splines: a principled approach","volume":"7","author":"Royson","year":"2007","journal-title":"Stata J"},{"key":"2022053122502073200_CIT0018","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1023\/B:EJEP.0000017659.80903.5f","article-title":"A 20-year ecological study of the temporal association between influenza and meningococcal disease","volume":"19","author":"Jensen","year":"2004","journal-title":"Eur J Epidemiol"},{"key":"2022053122502073200_CIT0019","doi-asserted-by":"crossref","first-page":"e0128580","DOI":"10.1371\/journal.pone.0128580","article-title":"Potential impact of co-infections and co-morbidities prevalent in Africa on influenza severity and frequency: a systematic review","volume":"10","author":"Cohen","year":"2015","journal-title":"PLoS One"},{"key":"2022053122502073200_CIT0020","doi-asserted-by":"crossref","first-page":"1257.e1","DOI":"10.1016\/j.cmi.2020.01.004","article-title":"Influenza increases invasive meningococcal disease risk in temperate countries","volume":"26","author":"Salomon","year":"2020","journal-title":"Clin Microbiol Infect"},{"key":"2022053122502073200_CIT0021","doi-asserted-by":"crossref","first-page":"3588","DOI":"10.1128\/IAI.00155-09","article-title":"Influenza A virus neuraminidase enhances meningococcal adhesion to epithelial cells through interaction with sialic acid-containing meningococcal capsules","volume":"77","author":"Rameix-Welti","year":"2009","journal-title":"Infect Immun"},{"key":"2022053122502073200_CIT0022","doi-asserted-by":"crossref","first-page":"B64","DOI":"10.1016\/j.vaccine.2009.04.061","article-title":"Meningococcal carriage and disease\u2014population biology and evolution","volume":"27","author":"Caugant","year":"2009","journal-title":"Vaccine"},{"key":"2022053122502073200_CIT0023","doi-asserted-by":"crossref","first-page":"e0120226","DOI":"10.1371\/journal.pone.0120226","article-title":"Evaluation of two influenza surveillance systems in South Africa","volume":"10","author":"Budgell","year":"2015","journal-title":"PLoS One"},{"key":"2022053122502073200_CIT0024","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1093\/infdis\/166.3.542","article-title":"Meningococcal disease and influenza-like syndrome: a new approach to an old question","volume":"166","author":"Hubert","year":"1992","journal-title":"J Infect Dis"},{"key":"2022053122502073200_CIT0025","doi-asserted-by":"crossref","first-page":"e360","DOI":"10.1016\/S2589-7500(21)00077-7","article-title":"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","volume":"3","author":"Brueggemann","year":"2021","journal-title":"Lancet Digit Heal"},{"key":"2022053122502073200_CIT0026","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1038\/d41586-020-03519-3","article-title":"How COVID-19 is changing the cold and flu season","volume":"588","author":"Jones","year":"2020","journal-title":"Nature"}],"container-title":["Clinical Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/cid\/advance-article-pdf\/doi\/10.1093\/cid\/ciab702\/40830934\/ciab702.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cid\/article-pdf\/74\/10\/1729\/43893792\/ciab702.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cid\/article-pdf\/74\/10\/1729\/43893792\/ciab702.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,31]],"date-time":"2022-05-31T22:54:41Z","timestamp":1654037681000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cid\/article\/74\/10\/1729\/6352205"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,14]]},"references-count":26,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2021,8,14]]},"published-print":{"date-parts":[[2022,5,30]]}},"URL":"https:\/\/doi.org\/10.1093\/cid\/ciab702","relation":{},"ISSN":["1058-4838","1537-6591"],"issn-type":[{"value":"1058-4838","type":"print"},{"value":"1537-6591","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,5,15]]},"published":{"date-parts":[[2021,8,14]]}}}