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Influenza Vaccination Is Associated with Reduced Diabetes Care 1 Influenza Vaccination Is Daniel Modin,1 Brian Claggett,2 Lars Køber,3,4 Morten Schou,1,3 Associated With Reduced Jens Ulrik Stæhr Jensen,3,5 Scott D. Solomon,2 Orly Vardeny,6 Cardiovascular Mortality in Adults Filip Krag Knop,3,7 Susanne Dam Nielsen,3,8 Michael Fralick,9 With Diabetes: A Nationwide Christian Torp-Pedersen,10 Gunnar Gislason,1,3 and Cohort Study Tor Biering-Sørensen1,11 https://doi.org/10.2337/dc20-0229 1Department of Cardiology, Herlev and Gentofte Hospital, University of Copenhagen, Hellerup, Denmark 2Department of Medicine, Cardiovascular Med- icine Division, Brigham and Women’s Hospital, OBJECTIVE Harvard Medical School, Boston, MA Recent influenza infection is associated with an increased risk of atherothrombotic 3Department of Clinical Medicine, Faculty of events,including acutemyocardial infarction (AMI) andstroke. Little is known about Health and Medical Sciences, University of Copen- the association between influenza vaccination and cardiovascular outcomes in hagen, Copenhagen, Denmark 4Department of Cardiology, Rigshospitalet, Uni- patients with diabetes. versity of Copenhagen, Copenhagen, Denmark 5Respiratory Medicine Section, Department of RESEARCH DESIGN AND METHODS Internal Medicine, Herlev and Gentofte Hospital, University of Copenhagen, Hellerup, Denmark We used nationwide register data to identify patients with diabetes in Denmark 6 during nine consecutive influenza seasons in the period 2007–2016. Diabetes was Center for Chronic Disease Outcomes Research, Minneapolis VA Health Care System, and Uni- defined as use of glucose-lowering medication. Patients who were not 18–100 years versity of Minnesota, Minneapolis, MN old or had ischemic heart disease, heart failure, chronic obstructive lung disease, 7Center for Clinical Metabolic Research, Herlev CARDIOVASCULAR AND METABOLIC RISK cancer, or cerebrovascular disease were excluded. Patient exposure to influenza and Gentofte Hospital, University of Copenha- fl gen, Hellerup, Denmark vaccination was assessed before each in uenza season. We considered the 8Department of Infectious Disease, Rigshospitalet, outcomes of death from all causes, death from cardiovascular causes, and death University of Copenhagen, Copenhagen, Denmark from AMI or stroke. For each season, patients were monitored from December 9Sinai Health System and the Department of 1untilApril1thenextyear. Medicine, University of Toronto, Toronto, On- tario, Canada 10 RESULTS Department of Health, Science and Technology, Aalborg University and Departments of Cardiol- A total of 241,551 patients were monitored for a median of four seasons ogy and Epidemiology/Biostatistics, Aalborg Uni- (interquartile range two–eight seasons) for a total follow-up of 425,318 person- versity, Aalborg, Denmark 11 years. The vaccine coverage during study seasons ranged from 24 to 36%. During Department of Biomedical Sciences, Faculty of Health and Medical Sciences, University of Co- follow-up, 8,207 patients died of all causes (3.4%), 4,127 patients died of penhagen, Copenhagen, Denmark cardiovascular causes (1.7%), and 1,439 patients died of AMI/stroke (0.6%). After Corresponding author: Daniel Modin, danielmo- adjustment for confounders, vaccination was significantly associated with re- [email protected] duced risks of all-cause death (hazard ratio [HR] 0.83, P < 0.001), cardiovascular Received 4 February 2020 and accepted 28 May death (HR 0.84, P < 0.001), death from AMI or stroke (HR 0.85, P 5 0.028), and a 2020 reduced risk of being admitted to hospital with acute complications associated This article contains supplementary material online with diabetes (diabetic ketoacidosis, hypoglycemia, or coma) (HR 0.89, P 5 0.006). at https://doi.org/10.2337/figshare.12436376. © 2020 by the American Diabetes Association. CONCLUSIONS Readers may use this article as long as the work is fl properly cited, the use is educational and not for In patients with diabetes, in uenza vaccination was associated with a reduced risk fi fl pro t, and the work is not altered. More infor- of all-cause death, cardiovascular death, and death from AMI or stroke. In uenza mation is available at https://www.diabetesjournals vaccination may improve outcome in patients with diabetes. .org/content/license. Diabetes Care Publish Ahead of Print, published online July 9, 2020 2Influenza Vaccination and Diabetes Diabetes Care In recent years, it has become increas- provided are unrestricted and include pharmacies since 1995. The register con- ingly clear that the abrupt inflammatory primary, secondary, and tertiary care. At tains information on drug type (coded response associated with acute infection birth or immigration, all citizens are as- using the Anatomical Therapeutic Chem- maytrigger ischemiceventssuchasacute signed a unique personal identification ical Classification System [ATC]), date of myocardial infarction (AMI) or stroke number (PIN) (13). This PIN is used dispense, and the PIN of the recipient. (1,2). Patients with diabetes have an throughout the Danish civil registration The register is used for drug cost re- increased risk of developing atheroscle- system, including the health care system. imbursement and is accurate (19). Using rotic cardiovascular disease, and they The PIN allows for linkage of health and the National Prescription Register, we suffer an increased mortality from acute administrative data at the individual level identified all prescriptions filled in Den- myocardial infarction (AMI) and stroke and ensures complete follow-up (14). Data mark in the 6 months before the start of compared with their counterparts with- for this study were retrieved from several each season (December 1) for glucose- out diabetes (3,4). Over the last two nationwide registries. More details and lowering medication (ATC code: A10) (Fig. decades, studies have linked influenza an overview of the registries used in this 1). It is well established that influenza infection with an increased risk of both study may be found in Supplementary vaccination is beneficial for patients with AMI (2,5,6) and stroke (7). Because pa- Table 1. high-risk health conditions such as lung tients with diabetes have a high risk of disease, heart disease, or cancer. We there- AMI and stroke in addition to an increased Study Design and Diabetes Definition fore excluded patients with common high- susceptibility for influenza infection (8,9), We used a modified cohort design with a riskdiseaseinanattempttoisolatethe they may be at high risk of suffering acute season-specific approach to assess the effect of vaccination in diabetes. Hence, ischemic events secondary to influenza association between influenza vaccina- patients who were younger than 18 years infection. This prompts the question of tion and outcome. We assumed that a old, older than 100 years old, had ischemic whether influenza vaccination may pre- potential causal association between heart disease, heart failure, chronic obstruc- vent cardiovascular mortality in patients vaccinationandimprovedoutcomewould tive pulmonary disease, cancer, or prior with diabetes. If this is the case, the safety be due to a reduced likelihood of in- cerebrovascular disease were excluded profile, cost efficiency, and feasibility of fluenza infection or a reduced severity of (Fig. 1). The inclusion process for the vaccination make it ideal for improving infection. Therefore, we confined our 2007–2008 season is presented in Fig. 1. outcomes in diabetes. main study period of interest to include An identical process was used to identify Currently, influenza vaccination is rec- months December, January, February, patients for the remaining eight seasons ommended for all patients with diabetes and March, because epidemiological data included in the study. by the American Diabetes Association in have shown that almost all influenza their Standards of Medical Care in Di- activity in Denmark occurs in these Patient Characteristics abetes 2019 guidelines (10). However, months (15). Consequently, if a potential Patient characteristics were assessed at this recommendation is made without a causal relationship between influenza the beginning of each season (Decem- class of recommendation and with a low vaccinationandoutcomeexists,thestron- ber 1). For more detail, we refer to the evidence level (level C, evidence based gest association is likely to be observed Supplementary Material. on observational studies of low quality) during this period. For the remainder of (10).Norandomizedcontrolledtrials thisreport,theperiodfromDecember1to Influenza Vaccination Status assessing the effect of influenza vacci- April 1 the following year (spanning the In Denmark, seasonal influenza vaccina- nation in patients with diabetes exist, 4monthsofhighinfluenza activity) will be tion is offered to all patients with di- and very little is known about the effect referred to as an influenza season. In this abetes free of charge. Records of vaccine of influenza vaccination on cardiovas- study, we considered all influenza seasons administration are recorded in the Gen- cular mortality in diabetes (11,12). Thus, in the period 2007–2016. Hence, we in- eral Practitioners Reimbursement Regis- whether influenza vaccination may pre- cluded nine seasons representing nine ter tied to the unique PIN of the vaccine vent cardiovascular mortality in diabetes distinct periods of observation. For each recipient. General practitioners are re- is not clear. Wetherefore soughtto assess season, we identified all patients living imbursed by the government for services the association between vaccination
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