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Data from UK Biobank John G Diabetes Care 1 Claire Welsh,1 Paul Welsh,1 Glycated Hemoglobin,Prediabetes, Carlos A. Celis-Morales,1 Patrick B. Mark,1 Daniel Mackay,2 Nazim Ghouri,1 and the Links to Cardiovascular Fredrick K. Ho,2 Lyn D. Ferguson,1 Rosemary Brown,1 James Lewsey,2 Disease: Data From UK Biobank John G. Cleland,2 Stuart R. Gray,1 2 2 https://doi.org/10.2337/dc19-1683 Donald M. Lyall, Jana J. Anderson, Pardeep S. Jhund,1 Jill P. Pell,2 Darren K. McGuire,3 Jason M.R. Gill,1 and Naveed Sattar 1 OBJECTIVE HbA1c levels are increasingly measured in screening for diabetes; we investigated whether HbA1c may simultaneously improve cardiovascular disease (CVD) risk assessment, using QRISK3, American College of Cardiology/American Heart Asso- ciation(ACC/AHA),andSystematicCOronaryRiskEvaluation(SCORE)scoringsystems. RESEARCH DESIGN AND METHODS UK Biobank participants without baseline CVD or known diabetes (n 5 357,833) were included. Associations of HbA1c with CVD was assessed using Cox models adjusting for classical risk factors. Predictive utility was determined by the C-index and net reclassification index (NRI). A separate analysis was conducted in 16,596 participants with known baseline diabetes. RESULTS Incident fatal or nonfatal CVD, as defined in the QRISK3 prediction model, occurred in 12,877 participants over 8.9 years. Of participants, 3.3% (n 5 11,665) had prediabetes (42.0–47.9 mmol/mol [6.0–6.4%]) and 0.7% (n 5 2,573) had un- diagnosed diabetes (‡48.0 mmol/mol [‡6.5%]). In unadjusted models, compared CARDIOVASCULAR AND METABOLIC RISK with the reference group (<42.0 mmol/mol [<6.0%]), those with prediabetes and undiagnosed diabetes were at higher CVD risk: hazard ratio (HR) 1.83 (95% CI 1.69– 1.97) and 2.26 (95% CI 1.96–2.60), respectively. After adjustment for classical risk factors, these attenuated to HR 1.11 (95% CI 1.03–1.20) and 1.20 (1.04–1.38), respectively.AddingHbA1c totheQRISK3 CVDrisk predictionmodel(C-index0.7392) yielded a small improvement in discrimination (C-index increase of 0.0004 [95% CI 0.0001–0.0007]). The NRI showed no improvement. Results were similar for models 1Institute of Cardiovascular & Medical Sciences, based on the ACC/AHA and SCORE risk models. University of Glasgow, Glasgow, U.K. 2Institute of Health & Wellbeing, University of CONCLUSIONS Glasgow, Glasgow, U.K. 3 The near twofold higher unadjusted risk for CVD in people with prediabetes is driven University of Texas Southwestern Medical Cen- ter, Dallas, TX mainly by abnormal levels of conventional CVD risk factors. While HbA adds 1c Corresponding author: Naveed Sattar, naveed minimally to cardiovascular risk prediction, those with prediabetes should [email protected] have their conventional cardiovascular risk factors appropriately measured and Received 21 August 2019 and accepted 27 Oc- managed. tober 2019 C.W. and P.W. are joint first authors. Circulating hemoglobin A1c (HbA1c) indicates average blood glucose concentrations © 2019 by the American Diabetes Association. over the preceding 3 months. The absence of the need for patients to fast for HbA Readers may use this article as long as the work is 1c properly cited, the use is educational and not for assessment is a major advantage of measuring HbA1c for screening for dysglycemia, profit, and the work is not altered. More infor- including diabetes and prediabetes, and has been endorsed for such screening mation is available at http://www.diabetesjournals by society recommendations (1). Whether screening HbA1c values incrementally .org/content/license. Diabetes Care Publish Ahead of Print, published online December 18, 2019 2 Prediabetes, HbA1c, and Cardiovascular Risk Diabetes Care contributes to cardiovascular disease conducted in accord with the principles AHA guideline prediction score including (CVD) risk assessment and prognostication of the Declaration of Helsinki. death from CVD (ICD-10 I20–25 and I60– beyond established risk predictors in pa- Systolic (SBP)and diastolic (DBP) blood 64) or hospitalization for CVD (ICD-10 I21, tients without diabetes remains uncer- pressure was taken as the first baseline I22, and I60–64) (5) (hereafter ACC/AHA tain, with meta-analysis of observational measurement, preferentially using an CVD events) and 2)fatalCVDasdefined by data suggesting independent prognostic automated measurement. Smoking sta- primary cause of death from events in- utility of HbA1c (2). tus was categorized into never or former/ cluded in the European SCORE clinical The European Systematic COronary current smoking. Ethnicity was coded as guidelines (I10–15, I44–51, I20–25, and Risk Evaluation (SCORE) CVD risk score white, black, South Asian, or mixed/ I61–73) (12) (hereafter SCORECVD events). (3), QRISK3 risk score (4), and the Amer- other, with white as the referent group. Endoffollow-upforeachparticipantwas ican College of Cardiology/American Blood collection sampling procedures for recorded as the date of death, the date of Heart Association (ACC/AHA) CVD risk the study have previously been described end of follow-up for the assessment center score (5) currently do not include any and validated (11). Biochemistry mea- attended (31 January 2018 for participants specific measure of glycemia in their risk sures were performed at a dedicated in England or Wales and 30 November prediction models and include only di- central laboratory on ;480,000 samples 2016forparticipantsinScotland),orthe abetes as a categorical entity. In support between 2014 and 2017. These included first date of CVD-related hospitalization of this approach, an individual partici- serum total cholesterol (TC) and HDL (for both composite fatal/nonfatal out- pant meta-analysis of nearly 300,000 cholesterol (HDL-C) (AU5400; Beckman comes)dwhichever came first. The pe- participants without diabetes or known Coulter) and plasma glycated hemoglo- riod at risk per participant began on the CVD at baseline suggested that HbA1c bin (HbA1c) (VARIANT II TURBO Hemo- date of their assessment. Participants added very modest discriminative ability globin Testing System; Bio-Rad). Data with baseline CVD were excluded from to CVD risk estimation methods that use were adjusted by UK Biobank centrally all analyses, and those with baseline conventional risk factors (6). Moreover, before release to adjust for preanalytical diabetes were analyzed separately from some data suggest that individuals with variables. Further details of these meas- the main cohort. prediabetes are at significantly elevated urements, and of the data adjustments, CVD risk due in part to their modestly can be found in the UK Biobank online Statistical Analyses raised glycemia levels (7,8). However, showcase and protocol (http://www Log-transformed HbA1c was analyzed as a such work has been based on either .ukbiobank.ac.uk and https://biobank continuous variable and was categorized relatively small single cohorts or multiple .ndph.ox.ac.uk/showcase/showcase/docs/ using thresholds of ,42.0 mmol/mol cohorts with considerable interstudy biomarker_issues.pdf). (,6.0%) (normal/referent), 42.0–47.9 heterogeneity. The lack of data from a The definition of baseline diabetes mmol/mol (6.0–6.4%) (prediabetes), and single large cohort with consistent phe- included self-reported type 1 or type 2 $48.0 mmol/mol ($6.5%) (undiagnosed notyping of exposures and events is a diabetes and self-reported use of insulin. diabetes), as well as deciles of the distribu- limitation in interpreting the existing Statin and bloodpressure medication use tion. Classical CVD risk factors were ex- literature on this topic. This topic re- was also recorded from self-report. Base- pressedasmean(SD)ifsymmetrically quires better evidence to inform clinical line CVD was defined as self-reported distributed, median (interquartile range) if care. prior myocardial infarction, stroke, and skewed, and number (%) if categorical. The Capitalizing on the availability of data transient ischemic attack as well as hos- prediabetes category of HbA1c was further in the UK Biobank comprising several pital diagnoses including ICD-10 codes split into the following categories to examine hundred thousand participants including I20–24, I63–64, and G45. its relationship with CVD outcomes: 42.0– baseline HbA1c measures and capture of Date and cause of death were ob- 44.9 mmol/mol (6.0–6.2%) and 45.0–47.9 longitudinal clinical outcomes, we exam- tained from death certificates held by mmol/mol (6.3–6.4%). The distribution ined the prognostic utility of HbA1c for the National Health Service (NHS) Infor- of classical CVD risk factors by categories CVD in participants without prevalent mation Centre for participants from Eng- of HbA1c was assessed using ANOVA, a diabetes. land and Wales and the NHS Central Wilcoxon test for trend, or a x2 test. Register Scotland for participants from Associations of classical CVD risk factors RESEARCH DESIGN AND METHODS Scotland. Hospital admissions were iden- and HbA1c with CVD outcomes were also The UK Biobank recruited 502,536 par- tified via linkage to Health Episode Sta- tabulated using these methods. ticipants (age 37–73 years) from 22 as- tistics, the Patient Episode Database, and Univariable associations of categories sessment centers across the U.K. between the Scottish Morbidity Records. The main of HbA1c with outcomes of interest were April 2007 and December 2010. Baseline outcome of interest in the current study initially explored using Kaplan-Meier biological measurements were recorded reflected the outcome used in the methods. Associations of continuous and touch screen questionnaires were QRISK3 risk score (4), namely, fatal or and categorical HbA1c with outcomes of administered as previously described nonfatal coronary heart disease, ische- interest were investigated using Cox pro- (9,10). The UK Biobank received ethics mic stroke, or transient ischemic attack portional hazards models for each out- approval from the North West Multicen- (ICD-10 G45, I20–24, and I63–64) (here- come, adjusted for age, sex, ethnicity, ter Research Ethics Committee (reference after QRISK3 CVD events). There were total cholesterol and HDL-C, SBP, DBP, number 11/NW/03820).
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