1. Introduction
A horrific case load of COVID-19 cases swept across Brazil in the winter of 2021, leading to a pandemic surge among susceptible, un-boosted elderly individuals previously immunized with the inactivated virus vaccine, Coronovac (Sinovac Biotech/Butantan Institute, São Paulo, Brazil) [1]. By spring 2021, the outlook had improved considerably, with COVID-19 cases plummeting dramatically by mid-October [2]. By then, a considerable proportion of the population had been boosted by recent natural infection with the Delta strain of SARS CoV-2 and/or received a booster dose with the Pfizer-BioNTech BNT162b2 (Pfizer-BioNTech, Kalamazoo, MI, USA) mRNA vaccine. By late spring, the state of Rio de Janeiro (RJ), a region severely affected by the COVID-19 pandemic, was reporting zero hospital admissions due to COVID-19 [2]. This brief reprieve in respiratory virus infections was followed by an impactful and completely unexpected Influenza H3N2 epidemic which peaked by late November 2021 [3] and declined throughout December 2021, disappearing by early January 2022 at which time the SARS CoV-2 Omicron strain surged in RJ and throughout Brazil [4].
This little publicized out-of-season opportunistic influenza epidemic occurred during a temporary COVID-19 void in between massive Delta and Omicron SARS CoV-2 surges. We evaluated whether climate change and poor influenza immunization coverage contributed to the genesis of this perfect storm.
2. Materials and Methods
2.1. Calculation of weekly SARS CoV-2 case numbers
Data on the number of weekly confirmed state SARS CoV-2 cases from the epidemiologic weeks of July 4, 2021, to December 26, 2021, was obtained from the RJ State Health Department [2]. Confirmed cases were reported to the Health Department based on positive molecular and/or antigen tests identified through the public network of the Brazilian Single Unified Health System (SUS) hospitals, clinics and ambulatory settings, public and private testing sites, private clinics, hospitals, and pharmacies distributed throughout the state [2,4].
2.2. Calculation of weekly influenza case numbers
We calculated weekly state influenza case numbers based on weekly influenza hospitalizations reported to the RJ State Health Department [4] using CDC methodology [5]. The estimated influenza burden estimates that flu hospitalizations comprise 1.3% of total cases and deaths 0.1% of influenza cases [5].
2.3. SARS CoV-2 immunization coverage
We assessed SARS CoV-2 vaccination coverage in RJ, which represented the proportion of the state population over 12 years of age who had received either two doses of Sinovac-CoronaVac (Sinovac Biotech/Butantan Institute, São Paulo, Brazil), Oxford–AstraZeneca (AstraZeneca, Oxford, U.K./Fiocruz, RJ, Brazil), or Pfizer-BioNTech BNT162b2 (Pfizer-BioNTech, Kalamazoo, MI, USA) mRNA vaccines or one dose of the Janssen vaccine (Janssen Biotech, Inc., Horsham, PA, USA), all provided by SUS, which is the only health network through which individuals in Brazil received COVID immunizations. Data on SARS CoV-2 immunization coverage was obtained from the RJ State Health Department [2].
2.4. Influenza immunization coverage
Information about influenza immunization coverage was obtained from the RJ State Health Department [4]. Flu vaccination in Brazil is recommended for all individuals over 6 months of age [6]. Immunization coverage represented the proportion of individuals in RJ state who received one dose of influenza vaccine between May 2021 to August 2021, the annual period in which flu vaccines are provided for the state [6]. The vaccine administered in 2021 was a trivalent vaccine consisting of two type A influenza strains (Victoria/2570/2019 H1N1, Hong Kong/2671/2019 H3N2) and one type B strain (Washington/02/2019, wild type) [7].
2.5. Association between out-of-season influenza outbreak and climatic variations
To assess the possible association between the out-of-season influenza outbreak and climatic variations, we evaluated temperature measurements from ten representative weather stations distributed across the RJ state. These were weather stations Arraial do Cabo, Campos dos Goytacazes, Cambuci, Duque de Caxias, Macaé, Pico do Couto, Resende, Rio de Janeiro, Seropédica, and Valença. This data was available through the Brazilian National Institute of Meteorology [8] (Figure 1). Maximum and minimum temperatures in Celsius units recorded across RJ state for October and November from 2016 to 2021 were abstracted. For comparison of weather patterns over six years, a two-tailed t-test was performed comparing values for maximum and minimum temperatures for October and November in 2021 with the mean values for October and November for 2016 to 2020 for RJ state. A p-value less than 0.05 was considered statistically significant.