Publications by authors named "Patrick Ohlmann"

120 Publications

Incomplete Recovery From Takotsubo Syndrome Is a Major Determinant of Cardiovascular Mortality.

Circ J 2021 Apr 6. Epub 2021 Apr 6.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire.

Background: Although there is an apparent rapid and spontaneous recovery of left ventricular ejection fraction (LVEF) in patients with Takotsubo syndrome (TTS), recent studies have demonstrated a long-lasting functional impairment in those patients. The present study sought to evaluate the predictors of incomplete recovery following TTS and its impact on cardiovascular mortality.Methods and Results:Patients with TTS between 2008 and 2018 were retrospectively enrolled at 3 different institutions. After exclusion of in-hospital deaths, 407 patients were split into 2 subgroups according to whether their LVEF was >50% (recovery group; n=341), or ≤50% (incomplete recovery group; n=66) at the chronic phase. Multivariate logistic regression analysis found that LVEF (odds ratio [OR]: 0.94; 95% confidence interval [CI]: 0.91-0.98; P<0.001) and C-reactive protein levels (OR: 1.11; 95% CI: 1.02-1.22; P=0.02) at discharge were independent predictors of incomplete recovery. At a median follow up of 52 days, a higher cardiovascular mortality was evident in the incomplete recovery group (16% vs. 0.6%; P<0.001).

Conclusions: This study demonstrated that incomplete recovery after TTS is characterized by residual systemic inflammation and an increased cardiac mortality at follow up. Altogether, the present study findings determined that patients with persistent inflammation are a high-risk subgroup, and should be targeted in future clinical trials with specific therapies to attenuate inflammation.
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http://dx.doi.org/10.1253/circj.CJ-20-1116DOI Listing
April 2021

Discrepancy in Von Willebrand Abnormalities Between Degenerative and Functional Mitral Regurgitation.

Am J Cardiol 2021 Mar 14. Epub 2021 Mar 14.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Strasbourg, France.; UMR1260 INSERM, Nanomédecine Régénérative, Faculté de Pharmacie, Université de Strasbourg, Illkirch, France.

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http://dx.doi.org/10.1016/j.amjcard.2021.03.007DOI Listing
March 2021

Angiotensin II-induced upregulation of SGLT1 and 2 contributes to human microparticle-stimulated endothelial senescence and dysfunction: protective effect of gliflozins.

Cardiovasc Diabetol 2021 Mar 16;20(1):65. Epub 2021 Mar 16.

Regenerative Nanomedicine, Faculty of Pharmacy, UMR 1260, INSERM (French National Institute of Health and Medical Research), University of Strasbourg, 67000, Strasbourg, France.

Background: Sodium-glucose cotransporter 2 (SGLT2) inhibitors reduced cardiovascular risk in type 2 diabetes patients independently of glycemic control. Although angiotensin II (Ang II) and blood-derived microparticles are major mediators of cardiovascular disease, their impact on SGLT1 and 2 expression and function in endothelial cells (ECs) and isolated arteries remains unclear.

Methods: ECs were isolated from porcine coronary arteries, and arterial segments from rats. The protein expression level was assessed by Western blot analysis and immunofluorescence staining, mRNA levels by RT-PCR, oxidative stress using dihydroethidium, nitric oxide using DAF-FM diacetate, senescence by senescence-associated beta-galactosidase activity, and platelet aggregation by aggregometer. Microparticles were collected from blood of patients with coronary artery disease (CAD-MPs).

Results: Ang II up-regulated SGLT1 and 2 protein levels in ECs, and caused a sustained extracellular glucose- and Na-dependent pro-oxidant response that was inhibited by the NADPH oxidase inhibitor VAS-2780, the AT1R antagonist losartan, sotagliflozin (Sota, SGLT1 and SGLT2 inhibitor), and empagliflozin (Empa, SGLT2 inhibitor). Ang II increased senescence-associated beta-galactosidase activity and markers, VCAM-1, MCP-1, tissue factor, ACE, and AT1R, and down-regulated eNOS and NO formation, which were inhibited by Sota and Empa. Increased SGLT1 and SGLT2 protein levels were observed in the rat aortic arch, and Ang II- and eNOS inhibitor-treated thoracic aorta segments, and were associated with enhanced levels of oxidative stress and prevented by VAS-2780, losartan, Sota and Empa. CAD-MPs promoted increased levels of SGLT1, SGLT2 and VCAM-1, and decreased eNOS and NO formation in ECs, which were inhibited by VAS-2780, losartan, Sota and Empa.

Conclusions: Ang II up-regulates SGLT1 and 2 protein expression in ECs and arterial segments to promote sustained oxidative stress, senescence and dysfunction. Such a sequence contributes to CAD-MPs-induced endothelial dysfunction. Since AT1R/NADPH oxidase/SGLT1 and 2 pathways promote endothelial dysfunction, inhibition of SGLT1 and/or 2 appears as an attractive strategy to enhance the protective endothelial function.
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http://dx.doi.org/10.1186/s12933-021-01252-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7967961PMC
March 2021

The Effect of Transoesophageal Echocardiography on Treatment Change in a High-Volume Stroke Unit.

J Clin Med 2021 Feb 17;10(4). Epub 2021 Feb 17.

Division of Cardiovascular Medicine, Hôpital Civil, Strasbourg University Hospital, 67000 Strasbourg, France.

Background and purpose-current guidelines recommend the use of transesophageal echocardiography (TEE) in relation to cardio-embolic sources of stroke. Methods-by using an hospital-based cohort, we retrospectively analyzed consecutive patients with acute ischemic stroke (AIS), acute hemorrhagic stroke (AHS) and transient ischemic attack (TIA) who were admitted in Strasbourg Stroke Center, France between November 2017 to December 2018. TEE reports were screened for detection of potential cardiac sources of embolism and the subsequent change in medical management. We performed univariate and multivariate analyses to identify predictors of relevant TEE findings. Results-out of the 990 patients admitted with confirmed stroke, 432 patients (42.6%) underwent TEE. Patients with TEE were younger (62.8 ± 14.8 vs. 73.8, < 0.001), presented less comorbidities and lower stroke severity assessed by lower NIHSS (2 IQR (0-4) vs. 3 IQR (0-10), < 0.01) and Modified (1 IQR (0-1) vs. 1 (0-3), < 0.01). A total of 227 examinations (52.5%) demonstrated abnormal findings considered as potential cardiac sources of embolism and 31 examinations (7.1%) were followed by subsequent change in medical management. Age (HR: 0.948, 95% CI 0.923 to 0.974; < 0.001), previous AIS (HR: 3.542, 95% CI 1.290 to 9.722; = 0.01), previous TIA (HR: 7.830, CI 95% 2214 to 27,689; = 0.001) and superficial middle cerebral artery territory infarction (HR: 2.774, CI 95% 1.168-6.589; = 0.021) were strong independent predictors with change in medical management following TEE. Conclusions-additional TEE changed the medical course of stroke patients in 7.1% in a French high-volume stroke unit.
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http://dx.doi.org/10.3390/jcm10040805DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7922802PMC
February 2021

Life-threatening arrhythmias in anterior ST-segment elevation myocardial infarction patients treated by percutaneous coronary intervention: adverse impact of morphine.

Eur Heart J Acute Cardiovasc Care 2020 Oct 14. Epub 2020 Oct 14.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, BP 426, 67091 Strasbourg, France.

Aims: Important controversies remain concerning the determinants of life-threatening arrhythmias during ST-segment elevation myocardial infarction (STEMI) and their impact on late adverse events. This study sought to investigate which factors might facilitate ventricular tachycardia (VT) and ventricular fibrillation (VF), in a homogeneous population of anterior STEMI patients defined by abrupt left anterior descending coronary artery (LAD) occlusion and no collateral flow.

Methods And Results: The 967 patients, who entered into the CIRCUS (Does Cyclosporine ImpRove Clinical oUtcome in ST elevation myocardial infarction patients) study, were assessed for further analysis. Acute VT/VF was defined as VT (run of tachycardia >30 s either self-terminated or requiring electrical/pharmacological cardioversion) or VF documented by electrocardiogram or cardiac monitoring, during transportation to the cathlab or initial hospitalization. VT/VF was documented in 136 patients (14.1%). Patients with VT/VF were younger and had shorter time from symptom onset to hospital arrival. Site of LAD occlusion, thrombus burden, area at risk, pre-percutaneous coronary intervention Thrombolysis in Myocardial Infarction flow, and ST-segment resolution were similar to that of patients without VT/VF. There was no impact of VT/VF on left ventricular remodelling or clinical outcomes. By multivariate analysis, the use of morphine (odds ratio 1.71; 95% confidence interval (1.13-2.60); P = 0.012) was the sole independent predictor of VT/VF occurrence.

Conclusions: In STEMI patients with LAD occlusion, our findings support the view that morphine could favour severe ventricular arrhythmias.
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http://dx.doi.org/10.1093/ehjacc/zuaa005DOI Listing
October 2020

Electrocardiographic Strain Pattern Is a Major Determinant of Rehospitalization for Heart Failure After Transcatheter Aortic Valve Replacement.

J Am Heart Assoc 2021 Feb 17;10(3):e014481. Epub 2021 Jan 17.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire Nouvel Hôpital CivilCentre Hospitalier UniversitaireUniversité de Strasbourg Strasbourg France.

Background Electrocardiographic strain pattern (ESP) has recently been associated with increased adverse outcome in aortic stenosis and after surgical aortic valve replacement. Our study sought to determine the impact and incremental value of ESP pattern in predicting adverse outcome after transcatheter aortic valve replacement. Methods and Results A total of 585 patients with severe aortic stenosis (mean age, 83±7 years; men, 39.8%) were enrolled for transcatheter aortic valve replacement from November 2012 to May 2018. ESP was defined as ≥1-mm concave down-sloping ST-segment depression and asymmetrical T-wave inversion in the lateral leads. The primary end points of the study were all-cause mortality, rehospitalization for heart failure, myocardial infarction, and stroke. A total of 178 (30.4%) patients were excluded because of left bundle-branch block (n=103) or right bundle-branch block (n=75). Among the 407 remaining patients, 106 had ESP (26.04%). At a median follow-up of 20.00 months (11.70-29.42 months), no impact of electric strain on overall and cardiac death could be established. By contrast, incidence of rehospitalization for heart failure was significantly higher (33/106 [31.1%] versus 33/301 [11%]; <0.001) in patients with ESP. By multivariate analyses, ESP remained a strong predictor of rehospitalization for heart failure (hazard ratio, 2.75 [95% CI, 1.61-4.67]; <0.001). Conclusions In patients with aortic stenosis who were eligible for transcatheter aortic valve replacement, ESP is frequent and associated with an increased risk of postinterventional heart failure regardless of preoperative left ventricular hypertrophy. ESP represents an easy, objective, reliable, and low-cost tool to identify patients who may benefit from intensified postinterventional follow-up.
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http://dx.doi.org/10.1161/JAHA.119.014481DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7955442PMC
February 2021

Effective Orifice Area of Balloon-Expandable and Self-Expandable Transcatheter Aortic Valve Prostheses: An Echo Doppler Comparative Study.

J Clin Med 2021 Jan 7;10(2). Epub 2021 Jan 7.

Pôle d'Activité Médico-Chirurgicale Cardiovasculaire, Hôpitaux Universitaires de Strasbourg, 67000 Strasbourg, France.

Published data on the size-specific effective orifice area (EOA) of transcatheter heart valves (THVs) remain scarce. Here, we sought to investigate the intra-individual changes in EOA and mean transvalvular aortic gradient (MG) of the Sapien 3 (S3), CoreValve (CV), and Evolut R (EVR) prostheses both at short-term and at 1-year follow-up. The study sample consisted of 260 consecutive patients with severe aortic stenosis who underwent transcatheter aortic valve implantation (TAVI). EOAs and MGs were measured with Doppler echocardiography for the following prostheses: S3 23 mm ( = 74; 28.5%), S3 26 mm ( = 67; 25.8%), S3 29 mm ( = 20; 7.7%), CV 23 mm ( = 2; 0.8%), CV 26 mm ( = 15; 5.8%), CV 29 mm ( = 24; 9.2%), CV 31 mm ( = 9; 3.5%), EVR 26 mm ( = 22; 8.5%), and EVR 29 mm ( = 27; 10.4%). Values were obtained at discharge, 1 month, 6 months, and 1 year from implantation. At discharge, EOAs were larger and MGs lower for larger-size prostheses, regardless of being balloon-expandable or self-expandable. In patients with small aortic annulus size, the hemodynamic performances of CV and EVR prostheses were superior to those of S3. However, we did not observe significant differences in terms of all-cause mortality according to THV type or size. Both balloon-expandable and self-expandable new-generation THVs show excellent hemodynamic performances without evidence of very early valve degeneration.
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http://dx.doi.org/10.3390/jcm10020186DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7825656PMC
January 2021

Prognostic Value of Troponin Elevation in COVID-19 Hospitalized Patients.

J Clin Med 2020 Dec 17;9(12). Epub 2020 Dec 17.

Department of Hypertension, Vascular Disease and Clinical Pharmacology, Strasbourg Regional University Hospital, 67091 Strasbourg, France.

(1) Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) penetrates the respiratory epithelium through angiotensin-converting enzyme-2 (ACE2) binding. Myocardial and endothelial expression of ACE2 could account for the growing body of reported evidence of myocardial injury in severe forms of Human Coronavirus Disease 2019 (COVID-19). We aimed to provide insight into the impact of troponin (hsTnI) elevation on SARS-CoV-2 outcomes in patients hospitalized for COVID-19. (2) Methods: This was a retrospective analysis of hospitalized adult patients with the SARS-CoV-2 infection admitted to a university hospital in France. The observation period ended at hospital discharge. (3) Results: During the study period, 772 adult, symptomatic COVID-19 patients were hospitalized for more than 24 h in our institution, of whom 375 had a hsTnI measurement and were included in this analysis. The median age was 66 (55-74) years, and there were 67% of men. Overall, 205 (55%) patients were placed under mechanical ventilation and 90 (24%) died. A rise in hsTnI was noted in 34% of the cohort, whereas only three patients had acute coronary syndrome (ACS) and one case of myocarditis. Death occurred more frequently in patients with hsTnI elevation (HR 3.95, 95% CI 2.69-5.71). In the multivariate regression model, a rise in hsTnI was independently associated with mortality (OR 3.12, 95% CI 1.49-6.65) as well as age ≥ 65 years old (OR 3.17, 95% CI 1.45-7.18) and CRP ≥ 100 mg/L (OR 3.62, 95% CI 1.12-13.98). After performing a sensitivity analysis for the missing values of hsTnI, troponin elevation remained independently and significantly associated with death (OR 3.84, 95% CI 1.78-8.28). (4) Conclusion: Our study showed a four-fold increased risk of death in the case of a rise in hsTnI, underlining the prognostic value of troponin assessment in the COVID-19 context.
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http://dx.doi.org/10.3390/jcm9124078DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7766903PMC
December 2020

Risk and Severity of COVID-19 and ABO Blood Group in Transcatheter Aortic Valve Patients.

J Clin Med 2020 Nov 22;9(11). Epub 2020 Nov 22.

Division of Cardiovascular Medicine, Strasbourg University Hospital, 67000 Strasbourg, France.

While cardiovascular disease has been associated with an increased risk of coronavirus disease 2019 (COVID-19), no studies have described its clinical course in patients with aortic stenosis who had undergone transcatheter aortic valve replacement (TAVR). Numerous observational studies have reported an association between the A blood group and an increased susceptibility to SARS-CoV-2 infection. Our objective was to investigate the frequency and clinical course of COVID-19 in a large sample of patients who had undergone TAVR and to determine the associations of the ABO blood group with disease occurrence and outcomes. Patients who had undergone TAVR between 2010 and 2019 were included in this study and followed-up through the recent COVID-19 outbreak. The occurrence and severity (hospitalization and/or death) of COVID-19 and their associations with the ABO blood group served as the main outcome measures. Of the 1125 patients who had undergone TAVR, 403 (36%) died before 1 January 2020, and 20 (1.8%) were lost to follow-up. The study sample therefore consisted of 702 patients. Of them, we identified 22 cases (3.1%) with COVID-19. Fourteen patients (63.6%) were hospitalized or died of disease. Multivariable analysis identified the A blood group (vs. others) as the only independent predictor of COVID-19 in patients who had undergone TAVR (odds ratio (OR) = 6.32; 95% confidence interval (CI) = 2.11-18.92; = 0.001). The A blood group (vs. others; OR = 8.27; 95% CI = 1.83-37.43, = 0.006) and a history of cancer (OR = 4.99; 95% CI = 1.64-15.27, = 0.005) were significantly and independently associated with disease severity (hospitalization and/or death). We conclude that patients who have undergone TAVR frequently have a number of cardiovascular comorbidities that may work to increase the risk of COVID-19. The subgroup with the A blood group was especially prone to developing the disease and showed unfavorable outcomes.
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http://dx.doi.org/10.3390/jcm9113769DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7700222PMC
November 2020

A case of acute disseminate encephalomyelitis after SARS-CoV-2 related acute respiratory distress syndrome.

J Neuroradiol 2020 Nov 18. Epub 2020 Nov 18.

Division of Cardiovascular Medicine, University Hospital of Strasbourg, Strasbourg, France. Electronic address:

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http://dx.doi.org/10.1016/j.neurad.2020.11.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7673217PMC
November 2020

Impact of residual inflammation on myocardial recovery and cardiovascular outcome in Takotsubo patients.

ESC Heart Fail 2021 Feb 18;8(1):259-269. Epub 2020 Nov 18.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, BP 426, Strasbourg, 67091, France.

Aims: Recent insights have emphasized the importance of myocardial and systemic inflammation in Takotsubo syndrome (TTS). In a large registry of unselected patients, we sought to evaluate whether residual high inflammatory response (RHIR) could impact cardiovascular outcome after TTS.

Methods And Results: Patients with TTS were retrospectively included between 2008 and 2018 in three general hospitals. Three hundred eighty-five patients with TTS were split into three subgroups, according to tertiles of C-reactive protein (CRP) levels at discharge (CRP <5.2 mg/L, CRP range 5.2 to 19 mg/L, and CRP >19 mg/L). The primary endpoint was the impact of RHIR, defined as CRP >19 mg/L at discharge, on cardiac death or hospitalization for heart failure. Follow up was obtained in 382 patients (99%) after a median of 747 days. RHIR patients were more likely to have a history of cancer or a physical trigger. Left ventricular ejection fraction (LVEF) at admission and at discharge were comparable between groups. By contrast, RHIR was associated with lower LVEF at follow up (61.7% vs. 60.7% vs. 57.9%; P = 0.004) and increased cardiac late mortality (0% vs. 0% vs. 10%; P = 0.001). By multivariate Cox regression analysis, RHIR was an independent predictor of cardiac death or hospitalization for heart failure (hazard ratio: 1.87; 95% confidence interval: 1.08 to 3.25; P = 0.025).

Conclusions: Residual high inflammatory response was associated with impaired LVEF at follow up and was evidenced as an independent factor of cardiovascular events. All together, these findings underline RHIR patients as a high-risk subgroup, to target in future clinical trials with specific therapies to attenuate RHIR.
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http://dx.doi.org/10.1002/ehf2.12945DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7835625PMC
February 2021

Increased susceptibility to SARS-CoV-2 infection in patients with reduced left ventricular ejection fraction.

ESC Heart Fail 2021 02 18;8(1):380-389. Epub 2020 Nov 18.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, Strasbourg, France.

Aims: Cardiovascular disease has been recognized as a major determinant of coronavirus disease 2019 (COVID-19) vulnerability and severity. Angiotensin-converting enzyme (ACE) 2 is a functional receptor for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and is up-regulated in patients with heart failure. We sought to examine the potential association between reduced left ventricular ejection fraction (LVEF) and the susceptibility to SARS-CoV-2 infection.

Methods And Results: Of the 1162 patients with acute coronary syndrome (ACS) who underwent percutaneous coronary intervention between February 2014 and October 2018, we enrolled 889 patients with available clinical follow-up data. Follow-up was conducted by telephone interviews 1 month after the start of the French lockdown which began on 17 March 2020. Patients were divided into two groups according to LVEF <40% (reduced LVEF) (n = 91) or ≥40% (moderately reduced + preserved LVEF) (n = 798). The incidence of COVID-19-related hospitalization or death was significantly higher in the reduced LVEF group as compared with the moderately reduced + preserved LVEF group (9% vs. 1%, P < 0.001). No association was found between discontinuation of ACE-inhibitor or angiotensin-receptor blockers and COVID-19 test positivity. By multivariate logistic regression analysis, reduced LVEF was an independent predictor of COVID-19 hospitalization or death (odds ratio: 6.91, 95% confidence interval: 2.60 to 18.35, P < 0.001).

Conclusions: In a large cohort of patients with previous ACS, reduced LVEF was associated with increased susceptibility to COVID-19. Aggressive COVID-19 testing and therapeutic strategies may be considered for patient with impaired heart function.
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http://dx.doi.org/10.1002/ehf2.13083DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7753539PMC
February 2021

Clinical features of patients with acute coronary syndrome during the COVID-19 pandemic.

J Thromb Thrombolysis 2020 Nov 16. Epub 2020 Nov 16.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, 1 place de l'Hôpital, 67091, Strasbourg cedex, France.

Although a reduction in hospital admissions of acute coronary syndromes (ACS) patients has been observed globally during the coronavirus disease 2019 (COVID-19) pandemic, clinical features of those patients have not been fully investigated. The aim of the present analysis is to investigate the incidence, clinical presentation, and outcomes of patients with ACS during the COVID-19 pandemic. We performed a retrospective analysis of consecutive patients who were admitted for ACS at our institution between March 1 and April 20, 2020 and compared with the equivalent period in 2019. Admissions for acute myocardial infarction (AMI) reduced by 39.5% in 2020 compared with the equivalent period in 2019. Owing to the emergency medical services (EMS) of our region, all time components of ST-elevated myocardial infarction care were similar during the COVID-19 outbreak as compared with the previous year's dataset. Among the 106 ACS patients in 2020, 7 patients tested positive for COVID-19. Higher incidence of type 2 myocardial infarction (29% vs. 4%, p = 0.0497) and elevated D-dimer levels (5650 μg/l [interquartile range (IQR) 1905-13,625 μg/l] vs. 400 μg/l [IQR 270-1050 μg/l], p = 0.02) were observed in COVID-19 patients. In sum, a significant reduction in admission for AMI was observed during the COVID-19 pandemic. COVID-19 patients were characterized by elevated D-dimer levels on admission, reflecting enhanced COVID-19 related thrombogenicity. The prehospital evaluation by EMS may have played an important role for the timely revascularization for STEMI patients.
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http://dx.doi.org/10.1007/s11239-020-02340-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7668406PMC
November 2020

Outcomes of COVID-19 Hospitalized Patients Previously Treated with Renin-Angiotensin System Inhibitors.

J Clin Med 2020 Oct 28;9(11). Epub 2020 Oct 28.

Department of Hypertension, Vascular Disease and Clinical Pharmacology, Strasbourg Regional University Hospital, 67091 Strasbourg, France.

(1) Background: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) penetrates respiratory epithelium through angiotensin-converting enzyme-2 binding, raising concerns about the potentially harmful effects of renin-angiotensin system inhibitors (RASi) on Human Coronavirus Disease 2019 (COVID-19) evolution. This study aimed to provide insight into the impact of RASi on SARS-CoV-2 outcomes in patients hospitalized for COVID-19. (2) Methods: This was a retrospective analysis of hospitalized adult patients with SARS-CoV-2 infection admitted to a university hospital in France. The observation period ended at hospital discharge. (3) Results: During the study period, 943 COVID-19 patients were admitted to our institution, of whom 772 were included in this analysis. Among them, 431 (55.8%) had previously known hypertension. The median age was 68 (56-79) years. Overall, 220 (28.5%) patients were placed under mechanical ventilation and 173 (22.4%) died. According to previous exposure to RASi, we defined two groups, namely, "RASi" ( = 282) and "RASi-free" ( = 490). Severe pneumonia (defined as leading to death and/or requiring intubation, high-flow nasal oxygen, noninvasive ventilation, and/or oxygen flow at a rate of ≥5 L/min) and death occurred more frequently in RASi-treated patients (64% versus 53% and 29% versus 19%, respectively). However, in a propensity score-matched cohort derived from the overall population, neither death (hazard ratio (HR) 0.93 (95% confidence interval (CI) 0.57-1.50), = 0.76) nor severe pneumonia (HR 1.03 (95%CI 0.73-1.44), = 0.85) were associated with RASi therapy. (4) Conclusion: Our study showed no correlation between previous RASi treatment and death or severe COVID-19 pneumonia after adjustment for confounders.
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http://dx.doi.org/10.3390/jcm9113472DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7692895PMC
October 2020

High-grade atrioventricular block occurring during percutaneous closure of patent foramen ovale: a case report.

Eur Heart J Case Rep 2020 Aug 25;4(4):1-5. Epub 2020 Jun 25.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, BP 426 - 67091 Strasbourg, France.

Background : Percutaneous closure of patent foramen ovale (PFO) is recommended for patients presenting with PFO-related stroke. Acute high-grade conduction disturbances occurring during PFO closure procedure have not been previously reported.

Case Summary : We describe for the first time a case of reversible complete atrioventricular block which occurred during closure of a PFO.

Discussion : We hypothesized that the block was the result of atrioventricular node compression-likely caused by the right-atrial disc of the 35-mm PFO closure device. We suggest implanting smaller devices in order to prevent atrioventricular conduction disturbances.
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http://dx.doi.org/10.1093/ehjcr/ytaa141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7501918PMC
August 2020

Value of Cardiac Biomarkers in the Early Diagnosis of Takotsubo Syndrome.

J Clin Med 2020 Sep 15;9(9). Epub 2020 Sep 15.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, 67091 Strasbourg, France.

Background: Bedside diagnosis between Takotsubo syndrome (TTS) and ST elevation (STEMI) and non-ST elevation (NSTEMI) myocardial infarction remains challenging. We sought to determine a cardiac biomarker profile to enable their early distinction.

Methods: 1100 patients (TTS = 314, STEMI = 452, NSTEMI = 334) were enrolled in two centers. Baseline clinical and biological characteristics were compared between groups.

Results: At admission, cut-off values of BNP (B-type natriuretic peptide)/TnI (Troponin I) ratio of 54 and 329 distinguished respectively STEMI from NSTEMI, and NSTEMI from TTS. Best differentiation was obtained by the use of BNP/TnI ratio at peak (cut-of values of 6 and 115 discriminated respectively STEMI from NSTEMI, and NSTEMI from TTS). We developed a score including five parameters (age, gender, history of psychiatric disorders, LVEF, and BNP/TnI ratio at admission) enabling good distinction between TTS and STEMI (77% specificity and 92% sensitivity, AUC 0.93). For the distinction between TTS and NSTEMI, a four variables score (gender, history of psychiatric disorders, LVEF, and BNP at admission) achieved a good diagnostic performance (89% sensitivity, 85% specificity, AUC 0.94).

Conclusion: A distinctive cardiac biomarker profile enables at an early stage a differentiation between TTS and ACS. A four (NSTEMI) or five variables score (STEMI) permitted a better discrimination.
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http://dx.doi.org/10.3390/jcm9092985DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7564647PMC
September 2020

Periprocedural Predictors of New-Onset Conduction Abnormalities After Transcatheter Aortic Valve Replacement.

Circ J 2020 09 1;84(10):1875-1883. Epub 2020 Sep 1.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire.

Background: New-onset conduction abnormalities (CAs) following transcatheter aortic valve replacement (TAVR) are associated with hospital rehospitalization and long-term mortality, but available predictors are sparse. This study sought to determine clinical predictors of new-onset left bundle branch block (LBBB) and new permanent pacemaker (PPM) implantation in patients undergoing TAVR.Methods and Results:We enrolled 290 patients who received SAPIEN 3 (Edwards Lifesciences, Irvine, CA, USA; n=217) or Evolut R (Medtronic, Minneapolis, MN, USA; n=73) from a prospective registry at Nouvel Hôpital Civil, Strasbourg, France between September 2014 and February 2018. Of 242 patients without pre-existing LBBB, 114 (47%) experienced new-onset LBBB and/or new PPM implantation. A difference between membranous septal length and implantation depth (∆MSID) was the only predictor of CAs for both types of valves. In the multivariate analysis, PR interval and ∆MSID remained as sole predictors of CAs. The risk for adverse clinical events, including all-cause death, myocardial infarction, stroke, and heart failure hospitalization, was higher for patients with CAs as compared with patients without CAs (hazard ratio: 2.10; 95% confidence interval: 1.26 to 3.57; P=0.004).

Conclusions: Computed tomography assessment of membranous septal anatomy and implantation depth predicted CAs after TAVR with new-generation valves. Future studies are required to identify whether adjustment of the implantation depth can reduce the risk of CAs and adverse clinical outcomes.
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http://dx.doi.org/10.1253/circj.CJ-20-0257DOI Listing
September 2020

Staging Severity of COVID-19 according to Hemostatic Abnormalities (CAHA Score).

Thromb Haemost 2020 Dec 30;120(12):1716-1719. Epub 2020 Aug 30.

Division of Cardiovascular Medicine, Nouvel Hôpital Civil, Strasbourg University Hospital, Strasbourg, France.

This is the first study to show a stepwise increase in venous thrombotic events according to COVID-19 coagulopathy (COVID-19-associated hemostatic abnormalities [CAHA]) staging and lung injuries assessed by chest computed tomography. Excess mortality and/or transfer to intensive care unit according to CAHA staging.
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http://dx.doi.org/10.1055/s-0040-1715836DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7869051PMC
December 2020

Predictive Impact of Paravalvular Leak Assessments on Clinical Outcomes Following Transcatheter Aortic Valve Replacement.

Am J Cardiol 2020 11 25;135:181-182. Epub 2020 Aug 25.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Strasbourg, France; UMR1260 INSERM, Nanomédecine Régénérative, Faculté de Pharmacie, Université de Strasbourg, Illkirch, France. Electronic address:

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http://dx.doi.org/10.1016/j.amjcard.2020.08.006DOI Listing
November 2020

Impact of Opioid Analgesia and Inhalation Sedation Kalinox on Pain and Radial Artery Spasm during Transradial Coronary Angiography.

J Clin Med 2020 Aug 25;9(9). Epub 2020 Aug 25.

Pôle d'Activité Médico-Chirurgicale Cardiovasculaire, Hôpitaux Universitaires de Strasbourg, Université de Strasbourg, 67000 Strasbourg, France.

With respect to the transfemoral approach, transradial procedures enable a drastic reduction of bleeding events and are associated with a reduction of mortality. Radial artery spasm (RAS) is one of the most common complications and may lead to patient discomfort and procedural failure. Currently, there is no consensus on the optimal sedation protocol to avoid RAS. The aim of this study was to investigate the respective impact of opioids analgesia and inhalation sedation with a 50% nitrous oxide/oxygen premix (Kalinox) on pain and occurrence of RAS during transradial coronary procedures. Consecutive patients undergoing transradial coronary angiography were prospectively enrolled in one, single center observational study (Nouvel Hôpital Civil, Strasbourg, France). Patients received opioids analgesia or inhalation sedation with Kalinox. The primary endpoints of the study were the incidence of a pain scale ≥5/10 and the occurrence of RAS. The secondary endpoints were the incidence of side effects. A total of 325 patients were enrolled (185 in the opioids analgesia group, 140 in the Kalinox group). RAS and pain scale ≥5 rates were not significantly different in the opioids analgesia and Kalinox groups (respectively 13.5% vs. 10.0% and 16.2% vs. 11.4%). Headache was more frequently observed in the Kalinox group (6.4% vs. 0.0%; = 0.002). By multivariate analysis, female gender, BMI <25 kg/m, puncture difficulty, the use of plastic needle and 6F sheath were identified as independent predictors of RAS. Procedural inhalation sedation by Kalinox is as safe as opioids analgesia during transradial coronary angiography.
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http://dx.doi.org/10.3390/jcm9092747DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7564999PMC
August 2020

Short-Term Effects of Air Pollution on Coronary Events in Strasbourg, France-Importance of Seasonal Variations.

Med Sci (Basel) 2020 Aug 7;8(3). Epub 2020 Aug 7.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, 67091 Strasbourg, France.

The aim of this study, is to investigate the effects of a short-term exposure to air pollutants, as assessed by Nitrogen dioxide (NO), Particulate Matter PM and PM concentrations, on coronary event onsets in Strasbourg, France. An observational, analytical, retrospective, epidemiological study was conducted in Strasbourg between 1 January 2012 and 31 December 2014. Higher daily coronary events rates were evidenced when NO concentrations were measured above 40 µg/m (1.258 (95% CI 1.142-1.374) vs. 1.110 (95% CI 1.033-1.186); = 0.015). The NO concentration was higher than 30 µg/m for 677 days (61.8%). Higher daily coronary events rates were evidenced when NO concentrations were measured above 30 µg/m (1.208 (95% CI 1.128-1.289) vs. 1.067 (95% CI 0.961-1.172) = 0.009). A marked seasonality of NO, PM, and PM concentrations characterized by an increase during winter and a decrease during the summer could be established. The seasonality of coronary events was evidenced simultaneously. After adjustments were made to account for the time and the month, no independent impact of NO, PM or PM on daily coronary events could be demonstrated.
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http://dx.doi.org/10.3390/medsci8030031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7563343PMC
August 2020

Accordion phenomenon in the descending aorta during transcatheter aortic valve replacement followed by mesenteric ischaemia.

Eur Heart J 2020 08;41(29):2819

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, 1 place de l'Hôpital - 67091 Strasbourg, France.

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http://dx.doi.org/10.1093/eurheartj/ehz793DOI Listing
August 2020

Paradoxical Increase of Stroke in Patients with Defect of High Molecular Weight Multimers of the von Willebrand Factors following Transcatheter Aortic Valve Replacement.

Thromb Haemost 2020 Sep 29;120(9):1330-1338. Epub 2020 Jul 29.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, Strasbourg, France.

Background:  Stroke is a major cause of disability after transcatheter aortic valve replacement (TAVR) and stroke prediction models and data are crucially needed. Following TAVR, high molecular weight (HMW) multimers defect of von Willebrand factor (VWF) as assessed by closure time of adenosine diphosphate (CT-ADP) value > 180 seconds is an independent predictor of bleeding events. This study sought to identify predictors of ischemic neurological events in patients who underwent TAVR and the specific impact of HMW multimers defect of VWF.

Methods:  Patients were prospectively enrolled between November 2012 and May 2018 at our institution. The CT-ADP, a point-of-care measure of hemostasis, was assessed the day before and 24 hours after the procedures. The rate of ischemic stroke and transient ischemic attack (TIA) was recorded up to 30 days after the procedures.

Results:  Of 565 TAVR patients, ischemic stroke/TIA was observed in 21 (3.7%) patients within 30 days. Ischemic stroke/TIA was associated with major/life-threatening bleeding complications (MLBCs) (9 [43%] vs. 88 [16%],  = 0.002) and postprocedure CT-ADP > 180 seconds (10 [48%] vs. 116 [21%],  = 0.01). By multivariate analysis, MLBCs (odds ratio [OR]: 3.58; 95% confidence interval [CI]: 1.45-8.84;  = 0.006) and postprocedure CT-ADP > 180 seconds (OR: 3.38; 95% CI: 1.38-8.25;  = 0.008) were evidenced as independent predictors of ischemic stroke/TIA.

Conclusion:  MLBCs and CT-ADP > 180 seconds were identified as predictors for ischemic stroke or TIA. The present study suggests that the defects of HMW multimers of the VWFs may contribute not only to bleeding events but also to thrombotic events.
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http://dx.doi.org/10.1055/s-0040-1713424DOI Listing
September 2020

Impact of Incomplete Coronary Revascularization on Late Ischemic and Bleeding Events after Transcatheter Aortic Valve Replacement.

J Clin Med 2020 Jul 16;9(7). Epub 2020 Jul 16.

Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, Université de Strasbourg, 67000 Strasbourg, France.

Background: The impact of coronary artery disease (CAD) and revascularization by percutaneous coronary intervention (PCI) on prognosis in patients undergoing transcatheter aortic valve replacement (TAVR) remain debated. A dismal prognosis in patients undergoing PCI has been associated with elevated baseline SYNTAX score (bSS) and residual SYNTAX score (rSS). The objective was to investigate whether the degree of bSS and rSS impacted ischemic and bleeding events after TAVR.

Methods: bSS and rSS were calculated in 311 patients admitted for TAVR. The primary outcome was the occurrence of major adverse cardiac events (MACE), a composite endpoint of myocardial infarction, stroke, cardiovascular death, or rehospitalization for heart failure. The occurrence of late major/life-threatening bleeding complications (MLBCs) and each primary endpoint individually were the secondary endpoints.

Results: bSS > 22 was associated with higher occurrence of MACE ( = 0.013). rSS > 8 and bSS > 22 had no impact on overall cardiovascular mortality. rSS > 8 and bSS > 22 were associated with higher rates of myocardial infarction ( = 0.001 and = 0.004) and late occurrence of MLBCs. Multivariate analysis showed that bSS > 22 (sHR 2.48) and rSS > 8 (sHR 2.35) remained predictors of MLBCs but not of myocardial infarction.

Conclusions: Incomplete coronary revascularization and CAD burden did not impact overall and cardiac mortality but constitute predictors of late MLBCs in TAVR patients.
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http://dx.doi.org/10.3390/jcm9072267DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7408638PMC
July 2020

Venous thromboembolism in non-critically ill patients with COVID-19 infection.

Thromb Res 2020 09 17;193:166-169. Epub 2020 Jul 17.

Division of Cardiovascular Medicine, Nouvel Hôpital Civil, Strasbourg University Hospital, Strasbourg, France; INSERM (French National Institute of Health and Medical Research), UMR 1260, Regenerative Nanomedicine, FMTS, Strasbourg, France. Electronic address:

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http://dx.doi.org/10.1016/j.thromres.2020.07.033DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7367026PMC
September 2020

Coronavirus Disease 2019: Associated Multiple Organ Damage.

Open Forum Infect Dis 2020 Jul 21;7(7):ofaa249. Epub 2020 Jun 21.

Service d'Anesthésie-Réanimation, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

A 56-year-old man presented a particularly severe and multisystemic case of coronavirus disease 2019 (COVID-19). In addition to the common lung and quite common pulmonary embolism and kidney injuries, he presented ocular and intestinal injuries that, to our knowledge, have not been described in COVID-19 patients. Although it is difficult to make pathophysiological hypotheses about a single case, the multiplicity of injured organs argues for a systemic response to pulmonary infection. A better understanding of physiopathology should feed the discussion about therapeutic options in this type of multifocal damage related to severe acute respiratory syndrome coronavirus 2.
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http://dx.doi.org/10.1093/ofid/ofaa249DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7336548PMC
July 2020

68Ga-DOTATOC PET for Treatment Efficacy Evaluation of Cardiac Sarcoidosis.

Clin Nucl Med 2020 Sep;45(9):e416-e418

Mallinckrodt Institute of Radiology, Division of Nuclear Medicine, Washington University, St Louis, MO.

Cardiac sarcoidosis (CS) has a poor prognosis related to life-threating arrhythmias and heart failure. Treatment includes anti-inflammatory therapies and implantable pacemaker and/or cardioverter defibrillator. The presence of cardiac devices and physiologic myocardial glucose uptake are major limitations of both cardiac magnetic resonance and F-FDG PET/CT, reducing their diagnostic value. Somatostatin-based PET/CT has been proposed to detect active CS. Contrarily to F-FDG uptake, which reflects nonspecific leukocyte infiltration, Ga-DOTATOC may identify active granulomatosis. Herein, we underline the specificity of Ga-DOTATOC PET in challeging clinical situations including refractory CS, and chronic CS in patients with cardiac device, or false-positive F-FDG PET/CT results.
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http://dx.doi.org/10.1097/RLU.0000000000003185DOI Listing
September 2020

Coronary Access and Percutaneous Coronary Intervention Up to 3 Years After Transcatheter Aortic Valve Implantation With a Balloon-Expandable Valve.

Circ Cardiovasc Interv 2020 07 25;13(7):e008972. Epub 2020 Jun 25.

King's College Hospital, London, United Kingdom (O.W.).

Background: Coronary artery disease and aortic stenosis often coexist. Transcatheter aortic valve implantation (TAVI) has emerged as a valid therapeutic option for younger, lower-risk patients who may eventually require coronary artery disease treatment. Thus, post-TAVI coronary access (CA) and percutaneous coronary intervention are expected to increase. The purpose of this study was to retrospectively evaluate patients who were enrolled in the SOURCE 3 (SAPIEN 3 Aortic Bioprosthesis European Outcome) European registry for treatment with the balloon-expandable SAPIEN 3 transcatheter heart valve and underwent CA with or without percutaneous coronary intervention after TAVI.

Methods: Baseline characteristics and clinical outcomes of patients with or without CA up to 3 years after TAVI were compared. A Kaplan-Meier estimate with a univariate model determined the impact of CA on cardiac mortality.

Results: Of 1936 TAVI patients (mean age 81.6 years, 52% male), 68 (3.5%) had CA within 3 years (mean 441±332 days) after TAVI. At baseline, the logistic EuroSCORE was similar (20.2% versus 18.3%, =0.2, CA and non-CA groups, respectively). Higher rates of coronary artery disease (76.5% versus 50.6%, <0.001), myocardial infarction (20.6% versus 11.5%, =0.03) and previous coronary artery bypass graft (22.1% versus 11.0%, =0.01) were present in the CA group. In 100% of patients, CA was successfully achieved. The clinical success of percutaneous coronary intervention was 97.9%. Cardiovascular mortality was numerically higher in patients with CA than in those without CA.

Conclusions: In the large SOURCE 3 European registry, CA was needed at 3-year follow-up after TAVI with a balloon-expandable valve in 3.5% of patients and was successful in all patients. The clinical success of percutaneous coronary intervention was 97.9%. Registration: URL: https://www.clinicaltrials.gov. Unique identifier: NCT02698956.
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http://dx.doi.org/10.1161/CIRCINTERVENTIONS.120.008972DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7373469PMC
July 2020

Long-term outcomes after acute myocardial infarction in patients with familial hypercholesterolemia: The French registry of Acute ST-elevation and non-ST-elevation Myocardial Infarction program.

J Clin Lipidol 2020 May - Jun;14(3):352-360.e6. Epub 2020 Apr 8.

Department of Pharmacology, Hôpital St Antoine, Université Pierre et Marie Curie, Paris, France.

Background: Patients with familial hypercholesterolemia (FH) are prone to develop acute myocardial infarction (AMI) at a younger age.

Objectives: The aim of the present study was to assess 5-year outcomes after AMI according to the presence of FH in a large multicenter cohort of patients.

Methods: The French registry of Acute ST-elevation and non-ST-elevation Myocardial Infarction consists of nationwide surveys recruiting patients over a 1- to 2-month period every 5 years. Patients recruited in 2005 and 2010 were followed up to 5 years.

Results: Of 5147 patients discharged alive and in whom FH status could be assessed, 2.8% had probable/definite FH, using an adapted Dutch Lipid Clinic score. They were 12 years younger, on average, than non-FH patients. Before adjustment, their 5-year survival and event-free survival did not differ from non-FH patients. After adjustment, however, both mortality (hazard ratio [HR] 1.82, 95% confidence interval [CI] 1.15-2.89; P = .011) and the combined endpoint of death, AMI, or stroke (HR 2.22, 95% CI: 1.51-3.26; P < .001) were higher in FH patients. The higher risk in FH patients was also present in patients receiving high-intensity lipid-lowering therapy at discharge: adjusted HR for mortality 2.29, 95% CI: 1.18 to 4.47, P = .015; HR for cardiovascular events 2.57, 95% CI: 1.48 to 4.48, P = .001. Concordant results were observed in propensity score-marched cohorts.

Conclusions: The risk of long-term mortality and cardiovascular events is twice as high in FH than in non-FH patients, when adjusted on baseline characteristics, even for those receiving high-intensity lipid-lowering therapy. Additional therapeutic measures are needed in these patients.
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http://dx.doi.org/10.1016/j.jacl.2020.03.008DOI Listing
April 2020

Impact of COVID-19 on the Cardiovascular System: A Review.

J Clin Med 2020 May 9;9(5). Epub 2020 May 9.

Université de Strasbourg, Pôle d'Activité Médico-Chirurgicale Cardio-Vasculaire, Nouvel Hôpital Civil, Centre Hospitalier Universitaire, 67091 Strasbourg, France.

The recent outbreak of coronavirus disease 2019 (COVID-19) caused by severe acute respiratory syndrome coronavirus 2 has been declared a public health emergency of international concern. COVID-19 may present as acute respiratory distress syndrome in severe cases, and patients with pre-existing cardiovascular comorbidities are reported to be the most vulnerable. Notably, acute myocardial injury, determined by elevated high-sensitivity troponin levels, is commonly observed in severe cases, and is strongly associated with mortality. Therefore, understanding the effects of COVID-19 on the cardiovascular system is essential for providing comprehensive medical care for critically ill patients. In this review, we summarize the rapidly evolving data and highlight the cardiovascular considerations related to COVID-19.
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http://dx.doi.org/10.3390/jcm9051407DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7291320PMC
May 2020