An unexpected inverse relationship between HbA 1c levels and mortality in patients with diabetes and advanced systolic heart failure

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1 An unexpected inverse relationship between levels and mortality in patients with diabetes and advanced systolic heart failure Shervin Eshaghian, MD, a Tamara B. Horwich, MD, b and Gregg C. Fonarow, MD, FACC b Los Angeles, CA Background In diabetes, poor glycemic control, as indexed by hemoglobin A1 c ( ), is associated with increased risk of cardiovascular events and new-onset heart failure (HF). However, in patients with diabetes and HF, the relationship between glucose control and survival has not been investigated. Our study aimed to evaluate the relationship between levels and mortality in patients with diabetes and advanced systolic HF. Methods We studied a cohort of 123 patients with diabetes and advanced systolic HF referred to a single center with values measured at presentation. The patients were grouped based on : V7.0 (n = 49) and N7.0 (n = 74). Results The cohort was 70% men, ejection fraction of 25% F 7, 59% ischemic etiology, 7.9 F 1.8, and diabetes duration of 8.6 F 9.0 years. The groups were similar in age; sex; New York Heart Association class; body mass index; diabetes duration; and insulin, metformin, and glitazone use. N7.0 was associated with higher ejection fraction, increased h-blocker, and sulfonlyurea use. Patients with V7.0 had significantly increased all-cause mortality, compared with those with N7.0 (35% vs 20%, hazard ratio 2.6, 95% CI , P b.01). In multivariate analysis, V7.0 remained associated with increased mortality (hazard ratio 2.3, 95% CI ). Conclusions Paradoxically, elevated levels were associated with improved survival in this cohort of patients with diabetes and advanced HF. Further investigation is necessary to determine the nature of this relationship and optimal in patients with diabetes and HF. (Am Heart J 2006;151:91.e1-91.e6.) Diabetes is associated with a substantially increased risk of new onset heart failure (HF). 1-3 Furthermore, several studies have shown that patients with HF with diabetes are at increased mortality risk compared with patients with HF without diabetes. 4,5 Heart failure may also predispose patients to the development of insulin resistance and new onset diabetes. 6,7 Hemoglobin A 1c ( ) is an index of metabolic control of diabetes. 8 Elevated levels of indicate poor metabolic control and are associated with microvascular and neuropathic complications. In patients with diabetes, lowering delays the onset and From the a Cedars Sinai Medical Center, Los Angeles, CA, and b Ahmanson-UCLA Cardiomyopathy Center, Los Angeles, CA. Submitted June 17, 2005; accepted October 16, The research was supported by the Ahmanson Foundation, Los Angeles, CA. Dr Horwich was funded by NIH training grant JI Dr Fonarow holds the Eliot Corday Chair in Cardiovascular Medicine and Science. Reprint requests: Gregg C. Fonarow, MD, FACC, Ahmanson-UCLA Cardiomyopathy Center, UCLA Division of Cardiology CHS , Le Conte Avenue, Los Angeles, CA gfonarow@mednet.ucla.edu /$ - see front matter n 2005, Mosby, Inc. All rights reserved. doi: /j.ahj slows the progression of these complications. 9,10 In addition, elevated levels are associated with increased risk in cardiovascular events. 11 Higher levels have also been associated with increased risk of new onset of HF in adult patients with diabetes. 12 Although poor glycemic control, as indexed by, is associated with increased risk of cardiovascular events and new-onset HF, the impact of on prognosis in patients with established systolic HF has not been previously investigated. Our study aimed to investigate the association between and survival in a large cohort of patients with advanced systolic HF of multiple etiologies. Methods Patient population The study population consisted of 123 consecutive patients with diabetes and advanced systolic HF referred to a single university medical center for HF management and/or transplant evaluation between 1995 and Patients with ejection fraction (EF) N40% and those b18 years old were excluded from the analysis. All patients were followed up in a comprehensive HF management program, as previously described. 13 The study protocol was approved by the UCLA Medical Institutional Review Board.

2 91.e2 Eshaghian, Horwich, and Fonarow American Heart Journal January 2006 Data collection Detailed information on patients baseline characteristics, including presence and duration of diabetes, were collected on initial assessment. Diabetes was defined by patient self-report and medical record documentation of diabetes. levels were measured within 6 weeks of initial referral. Medication and doses were recorded at initial visit. Laboratory testing, echocardiography, and right heart catherization occurred within 6 weeks of initial referral date. Body mass index (BMI) was calculated using the patients bdryq weight after empirical or pulmonary artery catheter guided HF therapy. Prior left heart catherization reports and angiographic films were reviewed, or if not done previously, left heart catherization was performed. Significant coronary artery disease was defined as any single stenosis N70% of the cross-section luminal diameter of the involved artery on angiography. End points All-cause mortality was the primary end point of the study. Heart transplantation (Status IA, IB, and II) was coded as a nonfatal end of follow-up at time of transplant, as previously described. 13 The composite end point of death or urgent transplant (status IA) was analyzed as a secondary end point. 14 Death was considered sudden if it was unexpected based on the patient s clinical status and if it occurred out of the hospital within 15 minutes of the onset of unexpected symptoms or during sleep. Death during hospitalization for worsening congestive symptoms was considered an HF death. Statistical analysis Patients were divided into 2 groups based on in serum: V7.0 (n = 49) and N7.0 (n = 74). Results are presented as mean F SD for continuous variables and percentage of total for categorical variables. Independentsamples t test, analysis of variance, and m 2 were used for comparison of variables, where appropriate. Both 1-year and 2-year survival curves were calculated by the Kaplan-Meier method, and differences between the curves were evaluated with the log-rank statistic. Survival was also assessed by quartile. Cox proportional hazards modeling was performed to analyze the association between, in addition to a variety of other prospectively recorded parameters and survival or urgent transplant-free survival. All of the variables listed in Tables I and II were considered as potential covariates. The sample size used in our study would allow the detection of a 20% absolute survival difference by Kaplan- Meier analysis between the 2 groups with a power of 80% with an a level of.05. Statistical Package for Social Sciences (SPSS) for Windows, Version 13.0 (Chicago, IL) was used for all analysis. Results Baseline characteristics of the cohort The cohort was 70% men, and ages ranged from 26 to 84 years (mean age 56 F 11 years). New York Heart Association III and IV HF comprised 42.9% and 41.2% of the population, respectively. Mean left ventricular EF Table I. Baseline characteristics of the study cohort Total cohort (n = 123) <_ 7.0 (n = 49) >7.0 (n = 74) P Age (y) 55.9 F F F Men (%) NYHA III-IV White (%) African American (%) Hispanic (%) EF (%) 24.9 F F F LVEDD (mm) 66.8 F F F Severe MR (%) Ischemic etiology (%) Smoking history (%) Hypertension (%) Diabetes 8.6 F F F duration (y) BMI (kg/m 2 ) 28.1 F F F Peak VO F F F (ml/kg per m) Systolic blood F F F pressure (mm Hg) PCWP (mm Hg) 15.8 F F F Cardiac index 2.8 F F F (L/mind m 2 ) Sodium F F F (mmol/l) BUN (mg/dl) 35.3 F F F Creatinine 1.58 F F F (mg/dl) Hemoglobin 12.6 F F F (g/dl) Cholesterol F F F (mg/dl) (%) 7.86 F F F LVEDD, Left ventricular end diastolic dimension; MR, mitral regurgitation; NYHA, New York Heart Association; VO 2, oxygen consumption; PCWP, pulmonary capillary wedge pressure; BUN, blood urea nitrogen. was 24.9 F 7.1 (Table I). Etiologies of HF were ischemic (59.3%), idiopathic (25.2%), and valvular (3.3%); the remaining etiologies included alcohol-induced, hypertrophic, and postpartum cardiomyopathy. There were 49 patients (39.8%) with V7.0 and 74 (60.2%) with N7.0. quartiles were Q1 (b6.6, n = 31), Q2 ( , n = 33), Q3 ( , n = 29), and Q4 (N8.9, n = 30). Mean duration of diabetes at the time of referral was 8.6 F 9.0 years. In this cohort of patients with diabetes and HF, 44 patients (35.8%) were treated with insulin (with or without oral glycemic control medications), 56 (45.5%) with oral glycemic control medications, and 23 (18.7%) exclusively treated with dietary modification. Differences in patient characteristics among those with

3 American Heart Journal Volume 151, Number 1 Eshaghian, Horwich, and Fonarow 91.e3 Table II. Medications use in the study cohort Figure 1 Total cohort (n = 123) <_ 7.0 (n = 49) >7.0 (n = 74) P ACE inhibitor or ARB (%) h-blocker (%) Statin (%) Diet only (%) Insulin (%) Metformin (%) Sulfonylurea (%) Glitazone (%) ARB, Angiotensin receptor blocker. V7.0 and those with N7.0 were analyzed (Table I). There were no statistically significant differences between the 2 groups in age, sex, mitral regurgitation, ischemic etiology, smoking history, BMI, serum sodium, creatinine, blood urea nitrogen, hemoglobin, and total cholesterol levels. However, patients with N7.0 had higher EF. The frequency of cardiovascular and diabetic medication use is listed in Table II. There was statistically significantly lower use of h-blockers and sulfonylurea and a trend for lower use of angiotensin-converting enzyme (ACE) inhibitors and/or angiotensin receptor blockers in patients with V7.0. Relationship between HbA1 c and mortality There were 32 deaths during the 2-year follow-up, with 17 deaths by year 1 and 15 deaths during year 2. Of the 32 deaths, progressive HF deaths accounted for 15 (47%), whereas 8 (25%) deaths were sudden, 2 (6%) occurred secondary to myocardial infarction, and 7 (22%) occurred from unknown or other causes. Of the 123 patients followed up, 32 received heart transplants by the 2-year follow-up: 17 urgent and 15 elective status. There were no patients lost to follow-up. Patients with HF with V7.0 were found to have significantly impaired survival compared with patients with N7.0. Survival rates in patients with HF with V7.0 versus those with N7.0 were 70% versus 93% at 1 year ( P b.01) and 50% versus 75% at 2 years ( P b.01) (Figure 1). On univariate analysis, V7.0 predicted increased mortality risk (hazard ratio [HR] 2.6, 95% CI ). Patients with V7.0 were also at significantly increased risk for the combined end point of death or urgent transplantation. Urgent transplant-free survival was 53% versus 86% at 1 year ( P b.01) and 36% versus 68% at 2 years ( P b.01) for patients with V7 and with N7.0, respectively. Mortality at 2 years was significantly higher in the lower 2 quartiles Kaplan Meier survival analysis for advanced systolic heart failure patients with diabetes and V7.0 (n = 49) versus N7.0 (n = 74) during 2-year follow-up. Figure 2 Mortality rates by Kaplan-Meier analysis for advanced systolic patients with HF with diabetes at 2 years by quartiles. The number of events and the number of subjects in each quartile are shown above each bar. with quartile 3 patients having the lowest mortality as shown in Figure 2. V7.0 was associated with increased mortality independent of other covariates. Even after adjustment for age, sex, ischemic etiology, diabetes duration, EF, BMI, h-blocker, ACE inhibitor, and sulfonylurea use, V7.0 remained a significant predictor of increased mortality at 1 year (HR 3.0, 95% CI ) and at 2 years (HR 2.3, 95% CI ) (Table III). V7.0 was similarly associated with an increased risk of the composite end point of death or urgent

4 91.e4 Eshaghian, Horwich, and Fonarow American Heart Journal January 2006 Table III. Multivariate analysis of 1 and 2-year survival <_ 7.0 (n = 49) >7.0 (n = 74) 1-y death, n (%) 12 (24.5%) 5 (6.8%) 1-y KM mortality rate 30% 7% 1-y unadjusted HR (95% CI) 4.6 ( ) y multivariate HR4 (95% CI) 3.7 ( ) y death or urgent Tx [n (%)] 22 (44.9%) 10 (13.5%) 1-y KM mortality or urgent Tx rate 47% 14% 1-y unadjusted HR (95% CI) 4.1 ( ) y multivariate HR4 (95% CI) 3.0 ( ) y death, n (%) 17 (34.7%) 15 (20.3%) 2-y KM mortality rate 50% 25% 2-y unadjusted HR (95% CI) 2.6 ( ) y multivariate HR4 (95% CI) 2.3 ( ) y death or urgent Tx (n [%]) 28 (57.1) 21 (28.4) 2-y KM mortality or urgent Tx rate 64% 32% 2-y unadjusted HR (95% CI) 2.8 ( ) y multivariate HR a (95% CI) 2.6 ( ) 1.0 KM, Kaplan-Meier; Tx, transplant. 4Adjusted for age, sex, ischemic etiology, diabetes duration, EF, BMI, h-blocker, ACE inhibitor, and sulfonylurea use. transplantation, independent of other risk factors (Table III). Discussion This study suggests a previously unrecognized and counterintuitive relationship between and prognosis in patients with diabetes and HF. We observed that higher (N7.0), as compared with lower (V7.0), was associated with significantly better survival in this patient population with advanced systolic HF. Patients with V7.0 had a 4.1-fold increased risk of mortality after 1 year and 2.3-fold increased mortality risk after 2 years, as compared with patients with N7.0. The association between worsened prognosis and V7.0 was observed independent of age, sex, ischemic etiology, diabetes duration, EF, BMI, h-blocker, ACE inhibitor, or sulfonylurea use. Diabetes is a well-recognized independent risk factor for the development of HF. 1,2 Both HF and diabetes are believed to share pathophysiologic processes such as neurohumoral activation, endothelial dysfunction, and oxidative stress. 15,16 The reported prevalence of diabetes in the adult population is 4% to 6%. 17 In clinical trials, the reported range of diabetes in patients with HF is roughly 25% Moreover, the prevalence of diabetes is reported to be higher in registries of patients hospitalized for HF, ranging from 26% to 44% With an overall HF prevalence of 5 million, there are an estimated 1 to 2 million patients with both HF and diabetes in the United States. Diabetes, HF, and mortality Diabetes has been associated with increased mortality in patients with established systolic HF. Analyses from Studies of Left Ventricular Dysfunction (SOLVD) trial have demonstrated that diabetes serves as an independent risk factor for progression from asymptomatic left ventricular dysfunction to symptomatic HF as well as a risk factor for all-cause mortality in patients with symptomatic HF (relative risk [RR], 1.4). 18 Subsequent analysis revealed that this increased risk was limited to patients with ischemic HF etiology (RR 1.37). 24,25 In addition, the BEST also linked the diabetes-related mortality risk to ischemic disease. 19 In an analysis of the DIAMOND study, diabetes predicted mortality independent of HF etiology (RR 1.5). 26 These prior studies did not, however, assess the relationship between glycemic control and clinical outcome in patients with diabetes and HF. In the current study, HbA1 c levels V7.0 were associated with significantly decreased survival. The difference in survival was evident as early as 3 months and persisted during 2 years of follow-up. Although this relationship is counterintuitive, several paradoxical relationships between conventional cardiovascular risk factors and clinical outcomes in patients with established HF have previously been described. This so-called reverse epidemiology in HF has been observed for obesity, total cholesterol and lipoprotein levels, and systolic blood pressure. 27 In 1203 patients with moderate to severe HF, higher BMI was found to be associated with a better, not worse, 2-year survival. 28,29 These findings of an obesity paradox in HF have subsequently been corroborated in several other studies Moreover, studies of patients with HF have shown that higher, not lower, total cholesterol levels have significantly increased survival. 33,34 In addition, higher blood pressure has been linked to increased survival in patients with severe HF. 35,36 This reverse epidemiology has been described in other patient populations including those with end-stage renal disease on dialysis and in the elderly. 27 There are a variety of plausible explanations for the relationship between lower and adverse outcomes in patients with HF observed in this study. Patients with lower may be under greater catabolic stress from HF and have less metabolic reserve. In patients with diabetes and advanced systolic HF, levels may not be an accurate index of glycemic control. Activation of receptors of advanced glycation end products that results in a complex cascade of signal transduction that is believed to play an important pathophysiological role in diabetic micro- and macrovascular disease may induce mechanisms that are favorable once HF is established. Because patients with higher at referral were more likely to be treated with oral diabetes medications, it could be hypothesized

5 American Heart Journal Volume 151, Number 1 Eshaghian, Horwich, and Fonarow 91.e5 that oral diabetes medications confer cardiovascular benefits independent of glycemic control that reduce mortality risk in diabetic patients with HF. 37 There are too few patients in this study on individual oral diabetic medications to fully explore this potential explanation. It is possible that patients with lower were more prone to severe hypoglycemia, resulting in increased mortality risk. Alternately, lower may merely be a marker of patients with more advanced HF. In addition, cachexia has been identified as an independent risk factor of mortality in patients with advanced heart failure, and it is plausible that the patients with lower HbA1 c are in a wasting process, which could lead to a poor prognosis. 38 This study of level and outcomes in patients with systolic HF has preliminarily identified a relationship that is strikingly different from that observed in patients with diabetes but without established HF. If this finding is confirmed in additional studies, well-designed clinical trials will be needed to determine the optimal level in patients with diabetes and systolic HF. Study limitations We acknowledge several potential limitations of our study. The cohort is a select population of patients with advanced systolic HF referred to a single university center. levels were examined at only 1 point in time. We did not measure insulin levels or other parameters of diabetes severity/metabolic control. We did not assess the relationship between and progression of microvascular disease or other complications of diabetes. This should be the focus of additional studies. There were significant differences in baseline characteristics and HF treatments between the patient groups. Even after adjustment for multiple covariates including age, sex, coronary artery disease, medication profile, EF, BMI, and diabetes duration, V7.0 could still be a surrogate for other measured and unmeasured variables that reflect more severe HF. Furthermore, the relatively small number of fatal events limits the number of variables that can be included in the multivariate analysis. In addition, HbA1 c data were not blinded and may have influenced subsequent clinical decision making not only with regard to glucose control but also to intensity of overall risk modification. Therefore, whether the relationship between glycemic control and increased mortality is causative is unknown. Nevertheless, this study has identified a novel and previously unrecognized relationship between level and outcomes in patients with diabetes and advanced HF. Conclusions In this cohort of patients with advanced systolic HF and diabetes, V7.0 was found to be associated with significantly impaired survival. The present findings warrant further investigation into the relationship between glycemic control and prognosis in patients with HF. References 1. Kannel WB, McGee DL. Diabetes and cardiovascular disease: the Framingham study. JAMA 1979;241: He J, Ogden LG, Bazzano LA, et al. Risk factors for congestive heart failure in US men and women: NHANES I epidemiologic follow-up study. Arch Intern Med 2001;161: Nichols GA, Gullion CM, Koro CE, et al. The incidence of congestive heart failure in type 2 diabetes: an update. Diabetes Care 2004;27: Kannel WB, Hjortland M, Castelli WP. Role of diabetes in congestive heart failure: the Framingham study. Am J Cardiol 1974;34: Ho KK, Pinsky JL, Kannel WB, et al. The epidemiology of heart failure: the Framingham Study. J Am Coll Cardiol 1993; 22 (Suppl A):6A - 13A. 6. Tenenbaum A, Motro M, Fisman EZ, et al. Functional class in patients with heart failure is associated with the development of diabetes. Am J Med 2003;114: Swan JW, Anker SD, Walton C, et al. Insulin resistance in chronic heart failure: relation to severity and etiology of heart failure. J Am Coll Cardio 1997;30: American Diabetes Association. Standard of medical care for patients with diabetes mellitus. Diabetes Care 1998;21:S23 - S The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993;329: UK Prospective Diabetes Study (UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 1998;352: Swan JW, Anker SD, Walton C, et al. Insulin resistance in chronic heart failure: relation to severity and etiology of heart failure. J Am Coll Cardiol 1997;30: Iribarren C, Karter AJ, Go AS, et al. Glycemic control and heart failure among adult patients with diabetes. Circulation 2001;103: Fonarow GC, Stevenson LW, Walden JA, et al. Impact of a comprehensive heart failure management program on hospital readmission and functional status of patients with advanced heart failure. J Am Coll Cardiol 1997;30: Aaronson KD, Mancini DM. Mortality remains high for outpatient transplant candidates with prolonged (N6 months) waiting list time. J Am Coll Cardiol 1999;33: Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 2002; 287: Reaven GM, Lithell H, Landsberg L. Hypertension and associated metabolic abnormalities the role of insulin resistance and the sympathoadrenal system. N Engl J Med 1996;334: Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology and management. JAMA 2002; 287: Schindler DM, KAstis JB, Yusuf S, et al. Diabetes mellitus, a predictor of morbidity and mortality in the studies of left ventricular dysfunction (SOLVD) trials and registry. Am J Cardiol 1996;77:

6 91.e6 Eshaghian, Horwich, and Fonarow American Heart Journal January Domanski M, Krause-Steinrauf H, Deedwania P, et al. The effect of diabetes on outcomes of patients with advanced heart failure in the BEST. J Am Coll Cardiol 2003;42: Gustafsson I, Brendorp B, Seibaek M, et al. Influence of diabetes and diabetes-gender interaction on the risk of death in patients hospitalized with congestive heart failure. J Am Coll Cardiol 2004;43: Adams Jr KF, Fonarow G, Emerman C, et al. Characteristics and outcomes of patients hospitalized for heart failure in the United States: rationale, design, and preliminary observations from the first 100,000 cases in the Acute Decompensated Heart Failure National Registry (ADHERE). Am Heart J 2005;149: Krum H, Gilbert RE. Demographics and concomitant disorders in heart failure. Lancet 2003;362: Nichols GA, Hillier TA, Erbey JR, et al. Congestive heart failure in type 2 diabetes: prevalence, incidence, and risk factors. Diabetes Care 2001;24: Dries DL, Sweitzer NK, Drazner MH, et al. Prognostic impact of diabetes mellitus in patients with heart failure according to the etiology of left ventricular systolic dysfunction. J Am Coll Cardiol 2001;38: Das SR, Drazner MH, Yancy CW, et al. Effects of diabetes mellitus and ischemic heart disease on the progression from asymptomatic left ventricular dysfunction to symptomatic heart failure: a retrospective analysis from the Studies of Left Ventricular Dysfunction (SOLVD) Prevention trial. Am Heart J 2004;148: Gustafsson I, Brendrop B, Seibaek M, et al. Influence of diabetes and diabetes-gender interaction on the risk of death in patients hospitalized with congestive heart failure. J Am Coll Cardiol 2004; 43: Kalantar-Zadeh K, Block G, Horwich TB, et al. Reverse epidemiology of conventional cardiovascular risk factors in patients with chronic heart failure. J Am Coll Cardiol 2004;43: Horwich TB, Fonarow GC. The impact of obesity on survival in patients with heart failure. Heart Fail Monit 2002;3: Horwich TB, Fonarow GC, Hamilton MA, et al. The relationship between obesity and mortality in patients with heart failure. J Am Coll Cardiol 2001;38: Mosterd A, Cost B, Hoes AW, et al. The prognosis of heart failure in the general population: the Rotterdam Study. Eur Heart J 2001;22: Davos CH, Doehner W, Rauchhaus M, et al. Body mass and survival in patients with chronic heart failure without cachexia: the importance of obesity. J Card Fail 2003;9: Lissin LW, Gauri Aj, Froelicher VF, et al. The prognostic value of body mass index and standard exercise testing in male veterans with congestive heart failure. J Card Fail 2002;8: Horwich TB, Hamilton MA, MacLellan WR, et al. Low serum total cholesterol is associated with marked increase in mortality in advanced heart failure. J Card Fail 2002;8: Rauchhaus M, Clark AL, Doehner W, et al. The relationship between cholesterol and survival in patients with chronic heart failure. J Am Coll Cardiol 2003;42: Pulignano G, Del Sindaco D, Tavazzi L, et al. Clinical features and outcomes of elderly outpatients with heart failure followed up in hospital cardiology units: data from a large nationwide cardiology database (IN-CHF Registry). Am Heart J 2002;143: Poole-Wilson PA, Uretsky BF, Thygesen K, et al. Mode of death in heart failure: findings from the ATLAS trial. Heart 2003;89: Masoudi FA, Inzucchi SE, Wang Y, et al. Thiazolidinediones, metformin, and outcomes in older patients with diabetes and heart failure: an observational study. Circulation 2005;111: Anker SD, Ponikowski P, Varney S, et al. Wasting as an independent risk factor for mortality in chronic heart failure. Lancet 1997;349:

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