Publications by authors named "Muhammad Shahzeb Khan"

194 Publications

Meta-Analysis Comparing the Safety and Efficacy of Dual Versus Single Antiplatelet Therapy After Transcatheter Aortic Valve Implantation.

Am J Cardiovasc Drugs 2021 Feb 26. Epub 2021 Feb 26.

Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.

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http://dx.doi.org/10.1007/s40256-021-00466-wDOI Listing
February 2021

Association of Palliative Care Intervention with Health Care Use, Symptom Burden and Advance Care Planning in Adults with Heart Failure and Other Noncancer Chronic Illness.

J Pain Symptom Manage 2021 Feb 22. Epub 2021 Feb 22.

Cardiology Section, Department of Medicine, Boston VA Healthcare System, Boston, MA. Electronic address:

Context: Palliative care (PC) improves outcomes in noncancer illness. We hypothesized the benefit is driven by studies of heart failure (HF) patients exclusively versus studies of other noncancer illnesses.

Objectives: To assess difference in outcomes in trials with HF patients exclusively vs studies of other noncancer chronic illness.

Methods: We performed a meta-analysis of studies that assessed association of PC with hospital admissions, emergency department (ED) visits and advance care planning in noncancer chronic illness and compared studies of HF patients versus those with other noncancer chronic illness.

Results: Our analysis included 10 HF studies (n=4,057) and 16 non-HF studies (11 mixed conditions, 3 dementia, 2 COPD, n=10,235). PC led to reduction in hospital admissions in HF studies (OR=0.67 [95% CI=0.48-0.95]) but not in other noncancer illness studies (OR=0.86 [95% CI=0.62-1.21]). PC intervention was non-significant for change in ED visits in either HF (OR=0.70 [95% CI=0.38-1.28]) or other noncancer studies (OR=0.86 [95% CI=0.69-1.07]). Increase in advance care planning was noted in both HF (OR=4.29 [95% CI=1.44-12.76]) and other studies (OR=2.67 [95% CI=1.29-5.52]). Non-significant reductions in symptom burden were noted for both HF-studies and non-HF studies, though overall there was a significant improvement in symptom burden (weighted mean difference -1.15 [95% CI=-1.65, -0.65]). Similar results were noted when studies of mixed populations were excluded from the non-HF studies.

Conclusion: PC is particularly effective at reducing potentially unwanted hospital admissions for patients with HF compared to other noncancer illnesses. Our findings should further encourage efforts to increase PC access to HF patients.
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http://dx.doi.org/10.1016/j.jpainsymman.2021.02.017DOI Listing
February 2021

Left Ventricular Assist Device Implantation in Hypertrophic and Restrictive Cardiomyopathy: A Systematic Review.

ASAIO J 2021 Mar;67(3):239-244

From the Division of Cardiology, Westchester Medical Center and New York Medical College, Valhalla, NY.

Left ventricular assist device (LVAD) implantation in patients with advanced heart failure due to hypertrophic or restrictive cardiomyopathy (HCM/RCM) presents technical and physiologic challenges. We conducted a systematic review of observational studies to evaluate the utilization and clinical outcomes associated with LVAD implantation in patients with HCM/RCM and compared these to patients with dilated or ischemic cardiomyopathy (DCM/ICM). We searched MEDLINE, EMBASE, and Scopus from inception through May 2019 and included appropriate studies describing the use of an LVAD in patients with HCM/RCM. We identified six studies with a total of 2,766 patients with HCM/RCM and advanced heart failure, among whom 338 patients (12.2%) underwent LVAD implantation. In patients listed for transplant, the rate of LVAD implantation was significantly lower in patients with HCM/RCM compared to that in patients with DCM/ICM (4.4% vs. 18.2%, p < 0.001). Adverse clinical outcomes were significantly higher in HCM/RCM than in DCM/ICM, including operative/short-term mortality (14.0% vs. 9.0%), right ventricular failure (50.0% vs. 21.0%), infection (15.5% vs. 11.2%), bleeding (40.2% vs. 12.5%), renal failure (15.0% vs. 5.1%), stroke (5.0% vs. 2.4%), and arrhythmias (18.0% vs. 7.7%) (all p values <0.001).
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http://dx.doi.org/10.1097/MAT.0000000000001238DOI Listing
March 2021

Efficacy and safety for the achievement of guideline-recommended lower low-density lipoprotein cholesterol levels: a systematic review and meta-analysis.

Eur J Prev Cardiol 2020 Nov 28. Epub 2020 Nov 28.

Division of Cardiology, Department of Medicine, Johns Hopkins School of Medicine, 600 North Wolfe Street, Blalock 524-D1, Baltimore, MD 21287.

Aim: The 2018 American Heart Association/American College of Cardiology/Multi-Society Cholesterol Guidelines recommended the addition of non-statins to statin therapy for high-risk secondary prevention patients above a low-density lipoprotein cholesterol (LDL-C) threshold of ≥70 mg/dL (1.8 mmol/L). We compared effectiveness and safety of treatment to achieve lower (<70) vs. higher (≥70 mg/dL) LDL-C among patients receiving intensive lipid-lowering therapy (statins alone or plus ezetimibe or proprotein convertase subtilisin/kexin type 9 inhibitors).

Methods And Results: Eleven randomized controlled trials (130 070 patients), comparing intensive vs. less-intensive lipid-lowering therapy, with follow-up ≥6 months and sample size ≥1000 patients were selected. Meta-analysis was reported as random effects risk ratios (RRs) [95% confidence intervals] and absolute risk differences (ARDs) as incident cases per 1000 person-years. The median LDL-C levels achieved in lower LDL-C vs. higher LDL-C groups were 62 and 103 mg/dL, respectively. At median follow-up of 2 years, the lower LDL-C vs. higher LDL-C group was associated with significant reduction in all-cause mortality [ARD -1.56; RR 0.94 (0.89-1.00)], cardiovascular mortality [ARD -1.49; RR 0.90 (0.81-1.00)], and reduced risk of myocardial infarction, cerebrovascular events, revascularization, and major adverse cardiovascular events (MACE). These benefits were achieved without increasing the risk of incident cancer, diabetes mellitus, or haemorrhagic stroke. All-cause mortality benefit in lower LDL-C group was limited to statin therapy and those with higher baseline LDL-C (≥100 mg/dL). However, the RR reduction in ischaemic and safety endpoints was independent of baseline LDL-C or drug therapy.

Conclusion: This meta-analysis showed that treatment to achieve LDL-C levels below 70 mg/dL using intensive lipid-lowering therapy can safely reduce the risk of mortality and MACE.
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http://dx.doi.org/10.1093/eurjpc/zwaa093DOI Listing
November 2020

Natriuretic Peptide Plasma Concentrations and Risk of Cardiovascular Versus Non-Cardiovascular Events in Heart Failure with Reduced Ejection Fraction Insights from the PARADIGM-HF and ATMOSPHERE Trials.

Am Heart J 2021 Feb 20. Epub 2021 Feb 20.

Department of Medicine, University of Mississippi, Jackson, Mississippi, USA.

Background: N-terminal pro-B-type natriuretic peptide (NTproBNP) plasma concentrations are independent prognostic markers in patients with heart failure with reduced ejection fraction (HFrEF). Whether a differential risk association between NTproBNP plasma concentrations and risk of cardiovascular (CV) versus non-CV adverse events exists is not well known.

Objective: To assess if there is a differential proportional risk of CV versus non CV adverse events by NTproBNP plasma concentrations.

Methods: In this post hoc combined analysis of PARADIGM-HF and ATMOSPHERE trials, proportion of CV versus non-CV mortality and hospitalizations were assessed by NT-proBNP levels (<400, 400-999, 1000-1999, 2000-2999, and >3000 pg/ml) at baseline using Cox regression adjusting for traditional risk factors.

Results: 14,737 patients with mean age of 62±8 years (24% history of atrial fibrillation [AF]) were studied. For CV deaths, the event rates per 1000 patient-years steeply increased from 33.8 in the ≤400 pg/ml group to 142.3 in the ≥3000 pg/ml group, while the non-CV death event rates modestly increased from 9.0 to 22.7, respectively. Proportion of non CV deaths decreased across the 5 NT-proBNP groups (21.1%, 18.4%, 17.9%, 17.4%, and 13.7% respectively). Similar trend was observed for non-CV hospitalizations (46.4%, 42.6%, 42.9%, 42.0%, and 36.9% respectively). These results remained similar when stratified according to presence of AF at baseline and prior HF hospitalization within last 12 months.

Conclusion: The absolute CV event rates per patient years of follow up were greater and had higher stepwise increases than non-CV event rates across a broad range of NT-proBNP plasma concentrations indicating a differential risk of CV events at varying baseline NT-proBNP values. These results have implications for future design of clinical trials.
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http://dx.doi.org/10.1016/j.ahj.2021.02.015DOI Listing
February 2021

Functional outcomes with Carillon device over 1 year in patients with functional mitral regurgitation of Grades 2+ to 4+: results from the REDUCE-FMR trial.

ESC Heart Fail 2021 Feb 22. Epub 2021 Feb 22.

Warwick Medical School, University of Warwick, Coventry, CV4 7AL, UK.

Aims: The objective of this study was to compare functional outcomes through 1 year in patients with core-lab verified moderate to severe (Grades 2+ to 4+) functional mitral regurgitation (FMR) treated with the Carillon device or control in the blinded sham-controlled REDUCE-FMR (Carillon Mitral Contour System for Reducing Functional Mitral Regurgitation) study.

Methods And Results: The main outcomes of this analysis were the change in 6 min walk test (6MWT) distance, incidence of heart failure hospitalization or death, change in New York Heart Association (NYHA) class, and change in Kansas City Cardiomyopathy Questionnaire (KCCQ) score through 1 year of follow-up. The minimum clinically important difference (MCID) was defined as a ≥30 m increase in 6MWT distance, an NYHA decrease in ≥1 class, and a ≥3 point increase in KCCQ score. The proportion of patients achieving the MCID in each treatment group was compared using Fisher's exact test, and the number needed to treat (NNT) with the Carillon device was calculated. Among 83 patients (62 Carillon and 21 sham), no statistically significant group differences were observed in the baseline characteristics. All outcomes at 1 year numerically favoured the Carillon group, including MCID for the 6MWT distance (59% vs. 23%, P = 0.029; NNT = 2.8), NYHA class (48% vs. 33%, P = 0.38; NNT = 6.9), KCCQ score (69% vs. 47%, P = 0.14; NNT = 4.5), and freedom from heart failure hospitalization or death (60% vs. 48%, P = 0.45; NNT = 8.3).

Conclusions: REDUCE-FMR was the first blinded sham-controlled trial to report outcomes with percutaneous therapy for the treatment of FMR. Trends towards improvement in mean 6MWT distance, KCCQ score, and NYHA class were observed with the Carillon device. A substantially higher number of patients achieved MCID for all patient-centred outcomes with the Carillon device compared with the sham procedure.
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http://dx.doi.org/10.1002/ehf2.13273DOI Listing
February 2021

Efficacy and safety of SGLT2 inhibitors in heart failure: systematic review and meta-analysis.

ESC Heart Fail 2020 Dec;7(6):3298-3309

Department of Cardiology (CVK) and Berlin Institute of Health Center for Regenerative Therapies (BCRT), German Centre for Cardiovascular Research (DZHK), partner site Berlin, Charité Universitätsmedizin Berlin, Augustenburger Platz 1, D-13353, Berlin, Germany.

Aims: We sought to conduct a meta-analysis regarding the safety and efficacy of sodium-glucose co-transporter 2 (SGLT2) inhibitors in patients with heart failure (HF).

Methods And Results: MEDLINE, Scopus, Cochrane CENTRAL, and ClinicalTrials.gov were searched from their inception to November 2020 for placebo-controlled randomized controlled trials of SGLT2 inhibitors. Randomized controlled trials were selected if they reported at least one of the prespecified outcomes in patients with HF. Hazard ratios (HRs) or risk ratios and their corresponding 95% confidence intervals were pooled using a random-effects model. A total of seven trials including 16 820 HF patients (N = 8884 in the SGLT2 inhibitor arms; N = 7936 in the placebo arms) were included. In the overall HF cohort, SGLT2 inhibitors compared with placebo significantly reduced the risk of the composite endpoint of first HF hospitalization or cardiovascular death [HR: 0.77 (0.72-0.83); P < 0.001; I = 0%], time to first HF hospitalization [HR: 0.71 (0.64-0.78); P < 0.001; I = 0], cardiovascular mortality [HR: 0.87 (0.79-0.96); P = 0.005; I = 0%], and all-cause mortality [HR: 0.89 (0.82-0.96); P = 0.004; I = 0%]. Results remained consistent across HF-specific trials and according to diabetes mellitus status. A trend towards benefit was observed in patients with HF with preserved ejection fraction for the composite of HF hospitalization and cardiovascular death [HR: 0.80 (0.63-1.00); P = 0.05; I = 29%]. No increased risk of hypovolaemia, hyperkalaemia, and hypotension was seen with SGLT2 inhibitors compared with placebo.

Conclusions: SGLT2 inhibitors significantly improve cardiovascular outcomes including cardiovascular and all-cause mortality in patients with HF without an increased risk of serious adverse events. A trend towards benefit was observed in patients with HF with preserved ejection fraction.
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http://dx.doi.org/10.1002/ehf2.13169DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7755023PMC
December 2020

Ferric carboxymaltose for the treatment of iron-deficient heart failure patients: a systematic review and meta-analysis.

ESC Heart Fail 2020 Dec;7(6):3392-3400

Monash University, Australia.

Aims: Intravenous ferric carboxymaltose (FCM) has been shown to improve functional capacity and quality of life in iron deficient heart failure patients. However, FCM's effect on hospitalizations and mortality remains unclear as previous randomized controlled trials (RCTs) and their meta-analyses have been underpowered to detect significant differences. We sought to conduct an updated meta-analysis using recently published RCT data.

Methods And Results: Online databases were searched from inception until November 2020 for RCTs evaluating the effects of FCM on clinical outcomes in iron-deficient heart failure patients. Outcomes of interest included heart failure hospitalizations, all-cause mortality, and cardiovascular mortality. Meta-analysis was performed using a fixed-effect model and estimates were reported as odds ratios (ORs), hazard ratios, or rate ratios (RRs) along with corresponding 95% confidence intervals (CIs). A total of 1947 patients (n = 1062 in the FCM group; n = 885 in the placebo group) were included. FCM, compared with placebo, significantly reduced the risk of the composite endpoint of time to first heart failure hospitalization or cardiovascular death (hazard ratio = 0.76; 95% CI = 0.63-0.90; I = 55%). FCM also significantly reduced the risk of recurrent heart failure hospitalizations (RR = 0.68; 95% CI = 0.54-0.85; I = 71%) and recurrent cardiovascular hospitalizations (RR = 0.71; 95% CI = 0.59-0.86; I = 56%). However, FCM had no significant effect on the risk of all-cause (OR = 0.97; 95% CI = 0.73-1.28; I = 0%) or cardiovascular mortality (OR = 0.93; 95% CI = 0.69-1.27; I = 0%).

Conclusions: Ferric carboxymaltose reduces heart failure hospitalizations and cardiovascular hospitalizations with no beneficial effect on all-cause and cardiovascular mortality in iron-deficient heart failure patients. These findings reinforce the role of FCM as a therapeutic option in heart failure patients.
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http://dx.doi.org/10.1002/ehf2.13146DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7754952PMC
December 2020

Coronary artery aneurysms: outcomes following medical, percutaneous interventional and surgical management.

Open Heart 2021 Feb;8(1)

Heart and Vascular Institute, Cleveland Clinic, Cleveland, Ohio, USA

Background: Coronary artery aneurysms (CAAs) are increasingly diagnosed on coronary angiography; however, controversies persist regarding their optimal management. In the present study, we analysed the long-term outcomes of patients with CAAs following three different management strategies.

Methods: We performed a retrospective review of patient records with documented CAA diagnosis between 2000 and 2005. Patients were divided into three groups: medical management versus percutaneous coronary intervention (PCI) versus coronary artery bypass grafting (CABG). We analysed the rate of major cardiovascular and cerebrovascular events (MACCEs) over a period of 10 years.

Results: We identified 458 patients with CAAs (mean age 78±10.5 years, 74.5% men) who received medical therapy (N=230) or underwent PCI (N=52) or CABG (N=176). The incidence of CAAs was 0.7% of the total catheterisation reports. The left anterior descending was the most common coronary artery involved (38%). The median follow-up time was 62 months. The total number of MACCE during follow-up was 155 (33.8%); 91 (39.6%) in the medical management group vs 46 (26.1%) in the CABG group vs 18 (34.6%) in the PCI group (p=0.02). Kaplan-Meier survival analysis showed that CABG was associated with better MACCE-free survival (p log-rank=0.03) than medical management. These results were confirmed on univariate Cox regression, but not multivariate regression (OR 0.773 (0.526 to 1.136); p=0.19). Both Kaplan-Meier survival and regression analyses showed that dual antiplatelet therapy (DAPT) and anticoagulation were not associated with significant improvement in MACCE rates.

Conclusion: Our analysis showed similar long-term MACCE risks in patients with CAA undergoing medical, percutaneous and surgical management. Further, DAPT and anticoagulation were not associated with significant benefits in terms of MACCE rates. These results should be interpreted with caution considering the small size and potential for selection bias and should be confirmed in large, randomised trials.
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http://dx.doi.org/10.1136/openhrt-2020-001440DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7878141PMC
February 2021

A comparative analysis of premature heart disease- and cancer-related mortality in women in the USA, 1999-2018.

Eur Heart J Qual Care Clin Outcomes 2021 Feb 8. Epub 2021 Feb 8.

Department of Medicine, Division of Cardiology, Johns Hopkins School of Medicine, Baltimore, MD, USA.

Aims: To compare premature heart disease- and cancer-related deaths in women in the USA.

Methods And Results: We analysed the US national database of death certificates of women aged <65 from the Centers for Disease Control and Prevention Wide-ranging Online Data for Epidemiologic Research database between 1999 and 2018. We measured annual percentage changes (APCs) in age-adjusted mortality rates (AAMRs) and years of potential life lost per 100 000 persons due to heart disease and cancer. Overall, cancer was a more prevalent cause of premature death compared with heart disease. Between 1999 and 2018, the AAMRs decreased for both cancer (61.9/100 000 to 45.6/100 000) and heart disease (29.2/100 000 to 22.6/100 000). However, while APC in AAMR for cancer declined consistently over time, after an initial decline, APC in AAMR for heart disease increased between 2010 and 2018 [0.53 95% confidence interval (0.18-0.89)], with a significant rise in Midwest, medium/small metros, and rural areas after 2008. Compared with cancer, APC in AAMR for heart disease increased in women aged 25-34 years [2.24 (0.30-4.22); 2013-18) and 55-64 years [0.46 (0.13-0.80); 2009-13], as well as Non-Hispanic (NH) Whites [APC, 0.79 (0.46-1.13); 2009-18] and NH American Indian/Alaskan Native [2.71 (0.59-4.87); 2011-2018]. Consequently, the mortality gap between cancer and heart disease has narrowed from an AAMR of 32.7/100 000 to 23.0/100 000.

Conclusions: The mortality gap between cancer and heart disease is decreasing among women <65 years. Intensive cardiovascular health interventions are required focusing on vulnerable young demographic subgroups and underserved regional areas to meet the American Heart Association's Impact Goal and Million Hearts Initiative.
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http://dx.doi.org/10.1093/ehjqcco/qcaa099DOI Listing
February 2021

Meta-Analysis of Efficacy of Sacubitril/Valsartan in Heart Failure With Preserved Ejection Fraction.

Am J Cardiol 2021 Jan 30. Epub 2021 Jan 30.

Division of Cardiology, Duke University School of Medicine, Durham, North Carolina; Duke Clinical Research Institute, Durham, North Carolina. Electronic address:

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http://dx.doi.org/10.1016/j.amjcard.2021.01.013DOI Listing
January 2021

Representation of women, older patients, ethnic, and racial minorities in trials of atrial fibrillation.

Pacing Clin Electrophysiol 2021 Jan 29. Epub 2021 Jan 29.

Department of Cardiovascular Medicine, Mayo Clinic, Rochester, Minnesota, USA.

Background: Representation trends of women, older adults, and ethnic/racial minorities in randomized controlled trials (RCTs) of atrial fibrillation (AF) are uncertain.

Methods: We systematically reviewed 134 AF related RCTs (phase II and III) encompassing 149,162 participants using Medline and ClinicalTrials.gov through April 2019 to determine representation trends of women, older patients (≥75 years), and ethnic/racial minorities. Weighted data on the prevalence of AF from epidemiological studies were used to compare the representation of the studied groups of interest in AF RCTs to their expected burden of the disease.

Results: Only 18.7% of the RCTs reported proportion of older patients, and 12.7% RCTs reported ethnic/racial minorities. The proportions of women in RCTs versus general population were 35.2% and 35.1%, of Hispanics were 11.9% and 5.2%, of Blacks were 1.2% and 5.7%, of American Indian/Alaskans were 0.2% and 0.2%, of Asians were 14.2% and 2.4%, of native Hawaiian/Pacific Islanders were 0.05% and 0.1% and of non-Whites were 19.5% and 22.5%, respectively. The weighted mean age (SD) across the trials was 65.3 (3.2) years which was less than the corresponding weighted mean age of 71.1 (4.5) years in the comparative epidemiological data.

Conclusion: The reporting of older patients and ethnic/racial minorities was poor in RCTs of AF. The representation of women and American Indian/Alaskan natives matched their expected population share of disease burden. Hispanics and Asians were over-represented and Blacks, native Hawaiian/Pacific Islanders and non-Whites were under-represented in RCTs of AF.
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http://dx.doi.org/10.1111/pace.14178DOI Listing
January 2021

Empagliflozin and health-related quality of life outcomes in patients with heart failure with reduced ejection fraction: the EMPEROR-Reduced trial.

Eur Heart J 2021 Jan 9. Epub 2021 Jan 9.

Cardiovascular Science, Baylor Heart and Vascular Institute, Baylor University Medical Center, 621 N. Hall Street, Dallas, TX 75226, USA.

Aims: In this secondary analysis of the EMPEROR-Reduced trial, we sought to evaluate whether the benefits of empagliflozin varied by baseline health status and how empagliflozin impacted patient-reported outcomes in patients with heart failure with reduced ejection fraction.

Methods And Results: Health status was assessed by the Kansas City Cardiomyopathy Questionnaires-clinical summary score (KCCQ-CSS). The influence of baseline KCCQ-CSS (analyzed by tertiles) on the effect of empagliflozin on major outcomes was examined using Cox proportional hazards models. Responder analyses were performed to assess the odds of improvement and deterioration in KCCQ scores related to treatment with empagliflozin. Empagliflozin reduced the primary outcome of cardiovascular death or heart failure hospitalization regardless of baseline KCCQ-CSS tertiles [hazard ratio (HR) 0.83 (0.68-1.02), HR 0.74 (0.58-0.94), and HR 0.61 (0.46-0.82) for <62.5, 62.6-85.4, and ≥85.4 score tertiles, respectively; P-trend = 0.10]. Empagliflozin improved KCCQ-CSS, total symptom score, and overall summary score at 3, 8, and 12 months. More patients on empagliflozin had ≥5-point [odds ratio (OR) 1.20 (1.05-1.37)], 10-point [OR 1.26 (1.10-1.44)], and 15-point [OR 1.29 (1.12-1.48)] improvement and fewer had ≥5-point [OR 0.75 (0.64-0.87)] deterioration in KCCQ-CSS at 3 months. These benefits were sustained at 8 and 12 months and were similar for other KCCQ domains.

Conclusion: Empagliflozin improved cardiovascular death or heart failure hospitalization risk across the range of baseline health status. Empagliflozin improved health status across various domains, and this benefit was sustained during long-term follow-up.

Clinical Trial Registration: URL: https://www.clinicaltrials.gov. Unique identifier: NCT03057977.
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http://dx.doi.org/10.1093/eurheartj/ehaa1007DOI Listing
January 2021

Effects of sodium-glucose cotransporter 1 and 2 inhibitors on cardiovascular and kidney outcomes in type 2 diabetes: A meta-analysis update.

Am Heart J 2021 Mar 29;233:86-91. Epub 2020 Dec 29.

Division of Cardiology, Department of Medicine, Duke University, Durham, NC; Duke Clinical Research Institute, Durham, NC. Electronic address:

In this report, we aim to provide an updated meta-analysis of the sodium-glucose cotransporter 2 (SGLT2) inhibitors trial data with the new trial data on sotagliflozin, a first-in-class dual SGLT1 and SGLT2 inhibitor. We searched Medline, Cochrane library, and Embase databases for randomized clinical trials comparing cardiovascular and kidney outcomes between SGLT2 and dual SGLT1/2 inhibitors and placebo. Nine randomized clinical trials with a total of 60,914 patients with type 2 diabetes were included. In patients with type 2 diabetes, the use of SGLT2 and dual SGLT1/2 inhibitors improves the cardiovascular and kidney outcome.
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http://dx.doi.org/10.1016/j.ahj.2020.12.007DOI Listing
March 2021

Major Depression and Anxiety Among Patients Hospitalized With Heart Failure.

Am J Cardiol 2021 03 28;142:153-155. Epub 2020 Dec 28.

Department of Medicine, University of Mississippi, Jackson, Mississippi.

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http://dx.doi.org/10.1016/j.amjcard.2020.12.053DOI Listing
March 2021

Cardiovascular implications of COVID-19 versus influenza infection: a review.

BMC Med 2020 12 18;18(1):403. Epub 2020 Dec 18.

Department of Medicine, University of Mississippi Medical Center, 2500 N. State Street, Jackson, MS, 39216, USA.

Background: Due to the overlapping clinical features of coronavirus disease 2019 (COVID-19) and influenza, parallels are often drawn between the two diseases. Patients with pre-existing cardiovascular diseases (CVD) are at a higher risk for severe manifestations of both illnesses. Considering the high transmission rate of COVID-19 and with the seasonal influenza approaching in late 2020, the dual epidemics of COVID-19 and influenza pose serious cardiovascular implications. This review highlights the similarities and differences between influenza and COVID-19 and the potential risks associated with coincident pandemics.

Main Body: COVID-19 has a higher mortality compared to influenza with case fatality rate almost 15 times more than that of influenza. Additionally, a significantly increased risk of adverse outcomes has been noted in patients with CVD, with ~ 15 to 70% of COVID-19 related deaths having an underlying CVD. The critical care need have ranged from 5 to 79% of patients hospitalized due to COVID-19, a proportion substantially higher than with influenza. Similarly, the frequency of vascular thrombosis including deep venous thrombosis and pulmonary embolism is markedly higher in COVID-19 patients compared with influenza in which vascular complications are rarely seen. Unexpectedly, while peak influenza season is associated with increased cardiovascular hospitalizations, a decrease of ~ 50% in cardiovascular hospitalizations has been observed since the first diagnosed case of COVID-19, owing in part to deferred care.

Conclusion: In the coming months, increasing efforts towards evaluating new interventions will be vital to curb COVID-19, especially as peak influenza season approaches. Currently, not enough data exist regarding co-infection of COVID-19 with influenza or how it would progress clinically, though it may cause a significant burden on an already struggling health care system. Until an effective COVID-19 vaccination is available, high coverage of influenza vaccination should be of utmost priority.
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http://dx.doi.org/10.1186/s12916-020-01816-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7746485PMC
December 2020

Reverse Cardiac Remodeling Following Initiation of Sacubitril/Valsartan in Patients With Heart Failure With and Without Diabetes.

JACC Heart Fail 2021 Feb 9;9(2):137-145. Epub 2020 Dec 9.

University of Mississippi, Jackson, Mississippi, USA. Electronic address:

Objective: This study sought to determine whether patients with heart failure and reduced ejection fraction (HFrEF) with type 2 diabetes mellitus (T2DM) have similar reverse cardiac remodeling with sacubitril/valsartan as patients without T2DM.

Background: Sacubitril/valsartan promotes reverse cardiac remodeling and improves outcomes in patients with HFrEF. Patients with HFrEF with T2DM have worse prognosis than those without T2DM.

Methods: In this post hoc analysis of PROVE-HF (Prospective Study of Biomarkers, Symptom Improvement, and Ventricular Remodeling During Sacubitril/Valsartan Therapy for Heart Failure), we examined changes in N-terminal pro-b-type natriuretic peptide (NT-proBNP), measures of cardiac remodeling, and Kansas City Cardiomyopathy Questionnaire Overall Summary (KCCQ-OS) scores from baseline to 12 months following initiation of sacubitril/valsartan between patients with HFrEF with and without T2DM. Using latent growth curve modeling, we evaluated the longitudinal association between changes in NT-proBNP, left ventricular ejection fraction, and KCCQ-OS.

Results: Among 794 patients enrolled, 361 (45.5%) had T2DM. NT-proBNP concentrations were modestly higher at baseline among patients with T2DM but were reduced after initiation of sacubitril/valsartan. Cross-sectional improvement was observed in left ventricular ejection fraction (T2DM: 28.3% at baseline and 37% at 12 months vs. non-T2DM: 28.1% at baseline and 38.3% at 12 months) and KCCQ-OS (T2DM: 71 at baseline and 83 at 12 months vs. non-T2DM: 76 at baseline and 88 at 12 months). Similar changes were also observed for other echocardiographic measures. In longitudinal analyses, the average NT-proBNP change was similar in patients with T2DM (-5.6% vs. -7.1% per 90-day interval; p = 0.64), whereas improvements in KCCQ-OS scores were slightly smaller (2.1 vs. 3.46 per 90-day interval; p = 0.07).

Conclusions: Sacubitril/valsartan favorably affects natriuretic peptide levels, reverse cardiac remodeling, and health status in patients with HFrEF with and without T2DM. (Effects of Sacubitril/Valsartan Therapy on Biomarkers, Myocardial Remodeling and Outcomes [PROVE-HF]; NCT02887183).
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http://dx.doi.org/10.1016/j.jchf.2020.09.014DOI Listing
February 2021

Sacubitril/valsartan for the management of heart failure: A perspective viewpoint on current evidence.

Int J Cardiol 2021 Mar 8;327:138-145. Epub 2020 Dec 8.

Department of Medicine, Department of Physiology and Pathophysiology, University of Manitoba, St Boniface Hospital, Winnipeg, Manitoba, Canada.

Current international guidelines recommend switching angiotensin converting enzyme inhibitors (ACE-i) or angiotensin receptor blockers (ARBs) to sacubitril/valsartan (S/V) in stable outpatients affected by heart failure with reduced ejection fraction (HFrEF) who remain symptomatic despite being on optimal medical therapy. Since these guidelines were published, new data may support further clinical applications and benefits of S/V beyond ambulatory HFrEF patients. The efficacy of S/V seems to be consistent across a wider array of subgroups including age, sex, etiology of HF, comorbidities, EF and estimated cardiovascular risk, with safety and tolerability profiles similar to ACE-I and ARBs. Additional clinical trial data are required to confirm the potential benefits of S/V in patients with mid-range or preserved EF, as suggested by analysis of PARAGON-HF, or in combination with sodium-glucose co-transporter 2 inhibitors or in post-myocardial infarction HF. In this article we summarize the new evidence on the effects and safety profile of S/V in HF and discuss current perspectives and persisting gaps. Currently, available evidence may support S/V as a first-line therapy in outpatient or in-hospital HFrEF patients, and possibly also in HFmrEF patients.
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http://dx.doi.org/10.1016/j.ijcard.2020.11.071DOI Listing
March 2021

Reporting and interpretation of subgroup analyses in heart failure randomized controlled trials.

ESC Heart Fail 2021 Feb 30;8(1):26-36. Epub 2020 Nov 30.

Department of Medicine, University of Mississippi, Jackson, MS, USA.

Aims: This study aimed to investigate the reporting of subgroup analyses in heart failure (HF) randomized controlled trials (RCTs) and to determine the strength and credibility of subgroup claims.

Methods And Results: All primary HF RCTs published in nine high-impact journals from 1 January 2008 to 31 December 2017 were included. Multivariable regression analysis was used to identify factors that may favour the reporting of results in specific subgroups. Strength of the subgroup effect claimed was classified into (i) strong, (ii) likely, or (iii) suggestive. Credibility of subgroup claim was scored using a pre-specified 10 pointer criteria. Of the 261 HF RCTs studied, 107 (41%) reported subgroup analyses. Twenty-five (23%) RCTs claimed a subgroup effect for the primary outcome of which six (24%) made a strong claim, eight (32%) claimed a likely effect, and 11 (44%) suggested a possible subgroup effect. Seven of the 25 RCTs did not employ interaction testing for subgroup claims of the primary outcome. Three out of 10 pre-specified credibility criteria were satisfied by half of the trials. Fourteen trials justified the choice of subgroups, and 10 explicitly stated they were underpowered to detect differences within subgroups. Source of funding did not influence the frequency of reporting subgroup analyses (OR 0.53, 95% CI 0.78-3.62, P = 0.52).

Conclusions: Appropriate credibility criteria were rarely met even by HF RCTs that held strong subgroup claims. Subgroup analyses should be pre-specified, be adequately powered, present interaction terms, and be replicated in independent data before being integrated into clinical decision making.
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http://dx.doi.org/10.1002/ehf2.13122DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7835611PMC
February 2021

Baseline characteristics of patients with heart failure with preserved ejection fraction in the EMPEROR-Preserved trial.

Eur J Heart Fail 2020 12;22(12):2383-2392

Baylor University Medical Center, Dallas, TX, USA.

Aims: EMPEROR-Preserved is an ongoing trial evaluating the effect of empagliflozin in patients with heart failure with preserved ejection fraction (HFpEF). This report describes the baseline characteristics of the EMPEROR-Preserved cohort and compares them with patients enrolled in prior HFpEF trials.

Methods And Results: EMPEROR-Preserved is a phase III randomized, international, double-blind, parallel-group, placebo-controlled trial in which 5988 symptomatic HFpEF patients [left ventricular ejection fraction (LVEF) >40%] with and without type 2 diabetes mellitus (T2DM) have been enrolled. Patients were required to have elevated N-terminal pro B-type natriuretic peptide (NT-proBNP) concentrations (i.e. >300 pg/mL in patients without and >900 pg/mL in patients with atrial fibrillation) along with evidence of structural changes in the heart or documented history of heart failure hospitalization. Among patients enrolled from various regions (45% Europe, 11% Asia, 25% Latin America, 12% North America), the mean age was 72 ± 9 years, 45% were women. Almost all patients had New York Heart Association class II or III symptoms (99.6%), and 23% had prior heart failure hospitalization within 12 months. Thirty-three percent of the patients had baseline LVEF of 41-50%. The mean LVEF (54 ± 9%) was slightly lower while the median NT-proBNP [974 (499-1731) pg/mL] was higher compared with previous HFpEF trials. Presence of comorbidities such as diabetes (49%) and chronic kidney disease (50%) were common. The majority of the patients were on angiotensin-converting enzyme inhibitors/angiotensin receptor blockers/angiotensin receptor-neprilysin inhibitors (80%) and beta-blockers (86%), and 37% of patients were on mineralocorticoid receptor antagonists.

Conclusion: When compared with prior trials in HFpEF, the EMPEROR-Preserved cohort has a somewhat higher burden of comorbidities, lower LVEF, higher median NT-proBNP and greater use of mineralocorticoid receptor antagonists at baseline. Results of the EMPEROR-Preserved trial will be available in 2021.
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http://dx.doi.org/10.1002/ejhf.2064DOI Listing
December 2020

The Changing Profile of Autopsies in Cardiovascular Deaths in the United States, 2003-2018.

Am J Cardiol 2021 02 23;140:150-151. Epub 2020 Oct 23.

Division of Cardiology, Johns Hopkins University School of Medicine, Baltimore, Maryland.

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http://dx.doi.org/10.1016/j.amjcard.2020.10.032DOI Listing
February 2021

Effect of sodium-glucose cotransporter 2 inhibitors on cardiovascular and kidney outcomes-Systematic review and meta-analysis of randomized placebo-controlled trials.

Am Heart J 2021 02 24;232:10-22. Epub 2020 Oct 24.

Division of Cardiology, Department of Medicine, Duke University, Durham, NC; Duke Clinical Research Institute, Durham, NC. Electronic address:

Sodium-glucose cotransporter 2 inhibitor (SGLT2i) use is associated with improved cardiovascular and kidney outcomes. However, the magnitude and potential heterogeneity of effect across patients with varying types of cardiometabolic and kidney disease is unclear. To examine the effect of SGLT2i on cardiovascular and kidney outcomes among patients with type 2 diabetes mellitus (T2DM), and independent of T2DM status, among patients with heart failure (HF), and chronic kidney disease.

Method: Medline, Embase, Cochrane library and scientific conferences were searched from inception till September 24, 2020 for randomized controlled trials comparing cardiovascular and kidney outcomes between SGLT2i and placebo. Random effects hazard ratios (HR) with 95% confidence intervals (CIs) were calculated.

Results: Eight trials with a combined 59,747 patients were included. In the overall population, SGLT2i reduced the risk of all-cause mortality (HR 0.84; 95% CI [0.78-0.91]), cardiovascular mortality (HR 0.84; 95% CI [0.76-0.93]) hospitalization for HF (HR 0.69; 95% CI [0.64-0.74]), myocardial infarction (HR 0.91; 95% CI [0.84-0.99]), and composite kidney outcome (HR 0.62; 95% CI [0.56-0.70]). There was no significant effect on the risk of stroke (HR 0.98; 95% CI [0.86-1.11]). Results were consistent across subgroups stratified by diabetes and HF status. SGLT2i use was not associated with a greater risk of hypoglycemia (OR 0.92; 95% CI [0.84-1.01]) or amputation (OR 1.25; 95% CI [0.97-1.62]). There were 64 diabetic ketoacidosis events with SGLT2i use and 18 with placebo (OR 2.86; 95% CI [1.39-5.86]).

Conclusions: In patients with cardiometabolic and kidney disease, SGLT2i improved cardiovascular and kidney outcomes, regardless of T2DM, HF, and/or CKD status. The magnitude of risk reduction was largest for hospitalization for HF and progression of kidney disease, more modest for mortality and MI and absent for stroke.
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http://dx.doi.org/10.1016/j.ahj.2020.10.064DOI Listing
February 2021

Discontinuation and non-publication of heart failure randomized controlled trials: a call to publish all trial results.

ESC Heart Fail 2021 Feb 15;8(1):16-25. Epub 2020 Nov 15.

Department of Medicine, University of Mississippi Medical Center, 2500 N. State Street, Jackson, MS, 39216, USA.

Aims: Discontinuation or non-publication of trials may hinder scientific progress and violates the commitment made to research participants. We sought to identify the prevalence of discontinuation and non-publication of heart failure (HF) clinical trials.

Methods And Results: We conducted a cross-sectional search of ClinicalTrials.gov to identify all completed and discontinued HF clinical trials. We limited our search to only include trials that were completed by 31 December 2017. Trials were investigated to identify reasons for discontinuation. Informative termination was defined as trial termination due to safety or efficacy concerns. Data pertaining to the trial phase, funding, intervention, enrolment, and trial completion date were extracted for each trial. A total of 572 trials were included. Of these, 21% (n = 118) were discontinued before completion. Patient accrual was the most frequently cited reason (n = 42; 36%) for trial discontinuation, followed by informative termination (n = 16; 14%) and funding (n = 14; 12%). Overall, 24 780 patients were enrolled in trials that were terminated. Of trials that were completed and not terminated, nearly one-third (n = 131/454; 29%) were not published. Seventy-nine (24%) trials were published within 12 months, 192 (59%) within 24 months, and 252 (78%) trials within 36 months.

Conclusions: Discontinuation and non-publication of HF trials is common. This raises ethical concerns towards participants who volunteer for research and are exposed to potential risks, inconvenience, and discomfort without furthering scientific progress.
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http://dx.doi.org/10.1002/ehf2.13099DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7835587PMC
February 2021

Effect of Empagliflozin on Cardiovascular and Renal Outcomes in Patients With Heart Failure by Baseline Diabetes Status: Results From the EMPEROR-Reduced Trial.

Circulation 2021 Jan 11;143(4):337-349. Epub 2020 Nov 11.

Baylor University Medical Center, Dallas, TX (M.P.).

Background: Sodium-glucose cotransporter 2 inhibitors improve outcomes in patients with heart failure with reduced ejection fraction, but additional information is needed about whether glycemic status influences the magnitude of their benefits on heart failure and renal events.

Methods: Patients with Class II-IV heart failure and a left ventricular ejection fraction ≤40% were randomized to receive empagliflozin (10 mg daily) or placebo in addition to recommended therapy. We prespecified a comparison of the effect of empagliflozin in patients with and without diabetes.

Results: Of the 3730 patients enrolled, 1856 (50%) had diabetes, 1268 (34%) had prediabetes (hemoglobin A1c [HbA1c] 5.7-6.4%), and 606 (16%) had normoglycemia (HbA1c <5.7%). The risks of the primary outcome (cardiovascular death or hospitalization for heart failure), total hospitalizations for heart failure, and adverse renal outcomes were higher in patients with diabetes, but were similar between patients with prediabetes and normoglycemia. Empagliflozin reduced the risk of the primary outcome in patients with and without diabetes (hazard ratio, 0.72 [95% CI, 0.60-0.87] and 0.78 [95% CI, 0.64-0.97], respectively, -interaction=0.57). Patients with and without diabetes also did not differ with respect to the effect of empagliflozin on total hospitalizations for heart failure, on the decline in estimated glomerular filtration rate over time, and on the risk of serious adverse renal outcomes. Among these end points, the effects of the drug did not differ in patients with prediabetes or normoglycemia. When analyzed as a continuous variable, baseline HbA1c did not significantly modify the benefits of empagliflozin on the primary outcome (-interaction=0.40). Empagliflozin did not lower HbA1c in patients with prediabetes or normoglycemia and was not associated with increased risk of hypoglycemia.

Conclusions: In EMPEROR-Reduced (Empagliflozin Outcome Trial in Patients With Chronic Heart Failure With Reduced Ejection Fraction), empagliflozin significantly improved cardiovascular and renal outcomes in patients with heart failure and a reduced ejection fraction, independent of baseline diabetes status and across the continuum of HbA1c. Registration: URL: https://www.clinicaltrials.gov; Unique identifier: NCT03057977.
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http://dx.doi.org/10.1161/CIRCULATIONAHA.120.051824DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7834911PMC
January 2021

The Time Is Now for Sodium Glucose Co-Transporter 2 Inhibitors for Heart Failure: A Call to Overcome Clinical Inertia.

Circ Heart Fail 2020 Dec 9;13(12):e008030. Epub 2020 Nov 9.

Division of Cardiology, Duke University School of Medicine, Durham, NC (S.J.G.).

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http://dx.doi.org/10.1161/CIRCHEARTFAILURE.120.008030DOI Listing
December 2020

BRASH Syndrome with Hyperkalemia: An Under-Recognized Clinical Condition.

Methodist Debakey Cardiovasc J 2020 Jul-Sep;16(3):241-244

COOK COUNTY HOSPITAL, CHICAGO, ILLINOIS.

BRASH syndrome is characterized by bradycardia, renal failure, use of an atrioventricular nodal blocker (AVNB), shock, and hyperkalemia. These symptoms represent an ongoing vicious cycle in a patient with a low glomerular filtration rate taking an AVNB. Decreased clearance of the medication and hyperkalemia associated with renal failure synergize to cause bradycardia and hypoperfusion. This reaction causes renal function to worsen, thereby perpetuating the cycle of BRASH syndrome.
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http://dx.doi.org/10.14797/mdcj-16-3-241DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7587309PMC
November 2020

Assessment of Heterogeneity in Heart Failure-Related Meta-Analyses.

Circ Heart Fail 2020 Nov 2;13(11):e007070. Epub 2020 Nov 2.

Heart and Vascular Center, Brigham and Women's Hospital, Boston, MA (M.V.).

Background: Assessment of heterogeneity in meta-analyses is critical to ensure the consistency of pooled results. Therefore, we sought to assess the evaluation and reporting of heterogeneity in heart failure (HF) meta-analyses.

Methods: Study level meta-analyses pertaining to HF were selected from January 2009 to July 2019, published in 11 high impact factor journals. We tabulated the overall proportion of the meta-analyses reporting statistical heterogeneity and specific metrics and methods employed to quantify and explore heterogeneity.

Results: Of 126 HF meta-analyses (612 outcomes), heterogeneity was reported for 422 outcomes (68.9 %) in 108 meta-analyses. Out of the 422 outcomes reporting statistical heterogeneity, 137 outcomes (32.5%) had no observable heterogeneity: (=0%), 40 outcomes (9.5%) had low heterogeneity (<25%), 76 outcomes (18%) had moderate heterogeneity (=25%-50%), and 169 outcomes (40%) had high heterogeneity (>50%). Reporting of statistical heterogeneity was not significantly associated with year of publication, funding source, disclosure information, or the type of studies pooled. Sensitivity analysis (n=68) was the most common statistical technique employed to evaluate the source of heterogeneity followed by subgroup analyses (n=59) and meta-regression (n=40).

Conclusions: Despite being an essential component of meta-analyses, heterogeneity was not reported for nearly 30% of outcomes and variably handled in contemporary HF meta-analyses. As meta-analyses increase across HF science, interpreting and handling of heterogeneity should be standardized.
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http://dx.doi.org/10.1161/CIRCHEARTFAILURE.120.007070DOI Listing
November 2020

Demographic, Regional, and State-Level Trends of Mortality in Patients With Aortic Stenosis in United States, 2008 to 2018.

J Am Heart Assoc 2020 11 19;9(21):e017433. Epub 2020 Oct 19.

Department of Cardiovascular Medicine Mayo Clinic Rochester MN.

Background Aortic stenosis-related mortality might vary across demographic subsets, regions, and states in the United States. Methods and Results We reviewed the death certificate data from the Centers for Disease Control and Prevention Wide-Ranging OnLine Data for Epidemiologic Research database to examine aortic stenosis-related mortality trends from 2008 to 2018. Crude and age-adjusted mortality rates (AAMRs) per 100 000 people and annual percentage change with 95% CIs were calculated. Between 2008 and 2018, AAMR reduced from 12.7 to 11.5 (average annual percentage change, -1.0 [95% CI, -1.5 to -0.5]), because of an accelerated decline between 2015 and 2018 (annual percentage change, -4.4 [95% CI, -6.0 to -2.7]). Older (aged >85 years), male, and White patients had higher death rates than younger, female, and non-White patients, respectively. Although mortality reduction was similar across sexes, significant mortality reduction was limited to White patients only. The AAMRs were higher in rural than urban areas. States with AAMRs >90th percentile were distributed in the West and the Northeast, and <10th percentile in the South. The AAMRs for sex and race were highest in the West and lowest in the South. None of the states located in the Midwest showed a significant reduction in mortality. Mortality remained stable for hospital setting and nursing home/long-term care facility, except that the number of deaths increased at home and hospice facility since 2014. Conclusions The reduction in mortality in patients with aortic stenosis was not consistent among demographic subsets and states. The substantial public health and economic implications call for determination of underlying clinical and socioeconomic factors to narrow the gap.
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http://dx.doi.org/10.1161/JAHA.120.017433DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7763421PMC
November 2020

What Makes Sodium-Glucose Co-Transporter-2 Inhibitors Stand out in Heart Failure?

Curr Diab Rep 2020 10 11;20(11):63. Epub 2020 Oct 11.

Heart and Vascular Center, Brigham and Women's Hospital Heart & Vascular Center and Harvard Medical School, 75 Francis St, Boston, MA, 02115, USA.

Purpose Of Review: We highlight the unique properties of the sodium-glucose cotransporter-2 (SGLT-2 inhibitors) which may lend favorably to their efficient integration in the background of other heart failure (HF) therapies. We also discuss the unique aspects of SGLT-2 inhibitor dosing, lack of titration needs, effects on kidney function and electrolytes, diuretic activity, and safety in the high-risk peri-hospitalization window.

Recent Findings: Dapagliflozin was recently approved for the treatment of heart failure with reduced ejection fraction (HFrEF), irrespective of the presence or absence of type 2 diabetes mellitus (T2DM) based on the findings of the pivotal DAPA-HF trial. All SGLT-2 inhibitors are once daily medications with minimal drug-drug interactions and do not require titration (for HF treatment) unlike other HF medications. SGLT-2 inhibitors offer modest weight loss and blood pressure reduction without major adverse effects of hyperkalemia, making it ideal for near-simultaneous initiation with other HF medications, and use in high-risk populations (including older adults). Moreover, SGLT-2 inhibitors appear to afford long-term kidney protection in diverse populations. SGLT-2 inhibitors are the latest class of therapies to demonstrate important clinical benefits among patients with HFrEF, and their pharmacological properties favor ease of use and integration in multi-drug disease-modifying regimens.
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http://dx.doi.org/10.1007/s11892-020-01347-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7548057PMC
October 2020