Influenza incidence, lineages, and vaccine effectiveness estimates in Lima, Peru, 2023
Authors: Juan Gonzalo Acevedo-Rodriguez, Carlos Zamudio, Noah Kojima, Fiorella Krapp, Pablo Tsukayama, Victor Giancarlo Sal y Rosas Celi, Dante Baldeon, Carmen Stefany Neciosup-Vera, Carlos Medina, Elsa Gonzalez-Lagos, Laura Castro, Ashley Fowlkes, Eduardo Azziz-Baumgartner, Eduardo Gotuzzo, Theresa Ochoa, Ericka Meza, Paula Arribas, Francesca Ginocchio, Flavia Morán, Renato Cava, Martina Guillermo, César Ugarte, Sol Abarca, Valeria Navarro, Roberto Freire-Esteves, Ashley Fowlkes
Journal: The Lancet Microbe (2024)

Characterisation of influenza viruses in the southern hemisphere can guide local response and provide insights to northern hemisphere jurisdictions about their upcoming influenza season.1Chard AN Nogareda F Regan AK et al.End-of-season influenza vaccine effectiveness during the southern hemisphere 2022 influenza season - Chile, Paraguay, and Uruguay.Int J Infect Dis. 2023; 134: 39-44Summary Full Text Full Text PDF PubMed Scopus (0) Google Scholar,2Barraza MF Fasce RA Nogareda F et al.Influenza incidence and vaccine effectiveness during the southern hemisphere influenza season - Chile, 2022.MMWR Morb Mortal Wkly Rep. 2022; 71: 1353-1358Crossref PubMed Google Scholar Here, we present the information on 2023 end of influenza season in the southern hemisphere about influenza lineages, incidence of medically attended, laboratory-confirmed influenza cases, and influenza vaccine effectiveness (VE) against the antigen from surveillance clinics and a hospital in San Juan de Lurigancho and San Martin de Porres, the two most populated districts of Peru. From Jan 1 to Sept 30, 2023, surveillance nurses sought individuals with COVID-19-like illness (CLI) of any age seeking care at outpatient sentinel sites between Monday and Saturday. CLI was defined as presenting with at least two of the following symptoms or signs—fever, chills, rigors, myalgia, headache, or sore throat for not more than 7 days from illness onset.3Centers for Disease Control and PreventionCoronavirus disease 2019 (COVID-19) 2021 case definition.https://ndc.services.cdc.gov/case-definitions/coronavirus-disease-2019-2021/Date: 2021Date accessed: August 25, 2023Google Scholar On March 7, 2023, the nurses expanded their search to CLI cases hospitalised for not more than 72 h at Cayetano Heredia National Hospital. Nurses obtained written consent to survey and swab CLI cases. Enrolled participants provided information on pre-existing conditions and influenza vaccination status. Individuals targeted for vaccination by Peru and vaccinated between Jan and Sept 2022, more than 14 days before enrolment, were considered vaccinated (appendix p 1). Nasopharyngeal swabs were obtained from individuals at the clinic. Anterior nasal and oral swabs were obtained from hospitalised patients. Specimens were tested for influenza and SARS-CoV-2 via multiplex quantitative PCR (qPCR).4Nagy A Černíková L Kunteová K et al.A universal RT-qPCR assay for "One Health" detection of influenza A viruses.PloS One. 2021; 16e0244669Crossref Scopus (19) Google Scholar Positive specimens with a cycle threshold value of 25 or less were sequenced by the Illumina Respiratory Virus Panel (Illumina, San Diego, CA, USA).5Sahajpal NS Mondal AK Njau A et al.High-throughput next-generation sequencing respiratory viral panel: a diagnostic and epidemiologic tool for SARS-CoV-2 and other viruses.Viruses. 2021; 13: 2063Crossref PubMed Scopus (5) Google Scholar We estimated the incidence of laboratory-confirmed influenza CLI by dividing the number of qPCR detections by the population assigned to the sentinel clinics by the Ministry of Health (ie, 91 801), adjusting for the proportion of CLI cases seeking care at sentinel versus other clinics in San Juan de Lurigancho and the proportion of CLI enrolled versus not enrolled (appendix pp 2–3). We calculated VE against medically attended influenza using a test-negative design.6Jackson ML Nelson JC The test-negative design for estimating influenza vaccine effectiveness.Vaccine. 2013; 31: 2165-2168Crossref PubMed Scopus (345) Google Scholar For this analysis, influenza cases were defined as qPCR influenza-positive CLI, whereas controls were defined as qPCR influenza-negative and SARS-CoV-2-negative CLI. Age, any pre-existing condition, and calendar year quarter were used to adjust VE. Surveillance activities were approved by the institutional review board of Universidad Peruana Cayetano (PRISA repository: EI0002439 and EI00002991) and the US Centers for Disease Control and Prevention as non-research (0900f3eb81ecbe9f and 0900f3eb820d72ac). During the surveillance period, 8688 individuals sought clinic care for respiratory illness. Surveillance nurses screened 1951 (22·5%) individuals, of whom 1196 (61·3%) met the CLI criteria and 732 (61·2%) were enrolled and swabbed (appendix p 4). Influenza was detected in 106 (14·5%) participants; 79 (75%) had type A influenza and 27 (25%) B influenza (appendix pp 5,7). Most (34 [87%] of 39) specimens with a cycle threshold value of 25 or less were sequenced and 30 (88%) of 34 belonged to influenza A(H1N1)pdm09 clade 6B.1A.5a.2a and 4 (12%) belonged to influenza A(H3N2) clade 3C.2a1b.2a.2a.3. No influenza B/Yamagata lineage viruses were identified. From March 7 to Sept 30, 2023, 12 (3·5%) of 342 hospitalised CLI cases were qPCR-positive for influenza type A, none were type B. The cumulative incidence of influenza CLI was 72·2 (95% CI 57·9 to 90·0) per 1000 population (appendix p 6); for participants enrolled at the clinic, 77 (10·5%) were vaccinated, 632 (86·3%) were not vaccinated, and 23 (3·1%) could not recall their vaccination status. The adjusted VE against medically attended influenza CLI at clinics was 51·8% (95% CI −5·7 to 78·0). During the 2023 influenza season in the southern hemisphere, we identified a higher incidence of influenza than that estimated by pre-COVID-19 Peruvian cohorts using the more specific influenza-like illness case definition—ie, 44 per 1000 person-years (95% CI 42·0 to 46·0).7Tinoco YO Azziz-Baumgartner E Uyeki TM et al.Burden of influenza in 4 ecologically distinct regions of Peru: household active surveillance of a community cohort, 2009–2015.Clin Infect Dis. 2017; 65: 1532-1541Crossref PubMed Scopus (0) Google Scholar Only one in ten enrolled participants from the clinic were vaccinated against seasonal influenza. Vaccinated individuals showed a 50% reduction in medically attended illnesses. The A/Victoria/2570/2019 (H1N1)pdm09-like virus antigen in the southern hemisphere vaccine formulation was effective in protecting against the predominant A(H1N1)pdm09 clade 6B.1A.5a.2a virus. Southern hemisphere 2023 influenza VE protection was similar to that of southern hemisphere 2022,1Chard AN Nogareda F Regan AK et al.End-of-season influenza vaccine effectiveness during the southern hemisphere 2022 influenza season - Chile, Paraguay, and Uruguay.Int J Infect Dis. 2023; 134: 39-44Summary Full Text Full Text PDF PubMed Scopus (0) Google Scholar,2Barraza MF Fasce RA Nogareda F et al.Influenza incidence and vaccine effectiveness during the southern hemisphere influenza season - Chile, 2022.MMWR Morb Mortal Wkly Rep. 2022; 71: 1353-1358Crossref PubMed Google Scholar US 2022–23, and early southern hemisphere 2023 seasons.8Fowlkes AL Nogareda F Regan A et al.Interim effectiveness estimates of 2023 southern hemisphere influenza vaccines in preventing influenza-associated hospitalizations - REVELAC-i network, March–July 2023.MMWR Morb Mortal Wkly Rep. 2023; 72: 1010-1015Crossref PubMed Scopus (1) Google Scholar Our findings have some limitations. Despite using a sensitive case definition, we probably missed non-respiratory influenza illnesses and underestimated influenza incidence. We relied on self-reported vaccination status and could not fully adjust our VE models for parameters associated with individuals' propensity to seek vaccination and care. Moreover, only half of the specimens had a cycle threshold value of 25 or less, and we might have missed emerging clades at the time of the evaluation. Our findings suggest that mostly unvaccinated people sought care early during the southern hemisphere season for illnesses that were predominantly attributable to influenza A(H1N1)pdm09 clade 6B.1A.5a.2a. Vaccinated individuals benefited from the A/Victoria/2570/2019 (H1N1)pdm09-like antigen, which conferred good protection against medically attended CLI. If similar viruses predominate in the northern hemisphere, our estimates of 2023 southern hemisphere influenza VE suggest that 2023–24 northern hemisphere influenza vaccines, which include similar H1N1 antigens, could provide similar protection during the upcoming northern hemisphere influenza season. JGAR has received support from the US CDC. CZ has received support from the US CDC and Pfizer as an international expert for an expert's symposia. FK has received support from the US CDC, grants or contracts from the Belgian Directorate of Development Cooperation, the Fogarty International Center of the US NIH, Pfizer as an international expert for an expert's symposia, Abbott as a key opinion leader advisory board member, and Peruvian Multisectoral Committee to combat antimicrobial resistance as an unpaid member. VGSRC has received support from the US CDC. EGL has received support from the US CDC, the Fogarty International Center of the US NIH, the University of Alabama at Birmingham for the Gorgas Advanced Course, Pfizer as an international expert to support an expert's symposia, the Peruvian Ministry of Health as an unpaid expert, and CFAR at the University of Washington Seattle as an unpaid member. All other authors declare no competing interests. This study was supported by the US Centers for Disease Control and Prevention cooperative agreement award GH00266. CZ and EG had full access to all the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis. FK, JGAR, CZ, VGSRC, FM, PT, EGL, and EG conceived and designed the study. EM coordinated laboratory analysis. PT performed genomic sequencing. PA, FG, SA, CM, VN, MG, and RC coordinated data collection and management. CSNV, DB, and VGSRC performed the statistical analysis. All authors wrote and approved the final manuscript. NK, FK, and EGL drafted, edited, and reviewed the manuscript. LC, AF, and EAB interpreted the findings and edited the manuscript. Data will be shared by the corresponding author upon reasonable request for research purposes. We recognise the contributions from several individuals and institutions to this project, including those from Dr Jorge Ponce, Dr Irma Hidalgo, and Mg Luz Nateros (Diris Lima Centro); Dr Roger Hernández and Dr Ana Quintana (Hospital Cayetano Heredia); Dr César Munayco (CDC Peru); Dr Anna Chard and Dr Sofía Arriola (CDC); and Dr Steev Loyola (Universidad Peruana Cayetano Heredia). The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the US Centers for Disease Control and Prevention. Download .pdf (.36 MB) Help with pdf files Supplementary appendix 1 Download .pdf (.07 MB) Help with pdf files Supplementary appendix 2