Publications by authors named "Can Ince"

350 Publications

Case Report: Early Identification of Subclinical Cardiac Tamponade in a Patient With a Left Ventricular Assist Device by the Use of Sublingual Microcirculatory Imaging: A New Diagnostic Imaging Tool?

Front Cardiovasc Med 2022 25;9:818063. Epub 2022 Mar 25.

Department of Cardiology, Unit Heart Failure, Heart Transplantation & Mechanical Circulatory Support, Erasmus Microcirculation (MC) University Medical Center Rotterdam, Rotterdam, Netherlands.

Clinical diagnosis of cardiac tamponade can be difficult in patients with continuous flow left ventricle assist devices (cf-LVADs). This is even more so because of the lack of adequate bedside echocardiographic windows. Previous studies on monitoring sublingual microcirculation showed deterioration of end-organ perfusion in patient with cardiogenic shock. In this paper we report alterations in the sublingual microcirculation in a cf-LVAD patient prior to clinical manifestation of tamponade. Our case report suggests that such real-time monitoring of the microcirculation may provide a new diagnostic modality for early recognition of cardiac tamponade.
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http://dx.doi.org/10.3389/fcvm.2022.818063DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8990877PMC
March 2022

Morphologic Mapping of the Sublingual Microcirculation in Healthy Volunteers.

J Vasc Res 2022 Mar 21:1-10. Epub 2022 Mar 21.

Department of Intensive Care, Erasmus MC, University Medical Center, Rotterdam, The Netherlands.

Purpose: Monitoring the sublingual and oral microcirculation (SM-OM) using hand-held vital microscopes (HVMs) has provided valuable insight into the (patho)physiology of diseases. However, the microvascular anatomy in a healthy population has not been adequately described yet.

Methods: Incident dark field-based HVM imaging was used to visualize the SM-OM. First, the SM was divided into four different fields; Field-a (between incisors-lingua), Field-b (between the canine-first premolar-lingua), Field-c (between the first-second premolar-lingua), Field-d (between the second molar-wisdom teeth-lingua). Second, we investigated the buccal area, lower and upper lip. Total/functional vessel density (TVD/FCD), focus depth (FD), small vessel mean diameters (SVMDs), and capillary tortuosity score (CTS) were compared between the areas.

Results: Fifteen volunteers with a mean age of 29 ± 6 years were enrolled. No statistical difference was found between the sublingual fields in terms of TVD (p = 0.30), FCD (p = 0.38), and FD (p = 0.09). SVMD was similar in Field-a, Field-b, and Field-c (p = 0.20-0.30), and larger in Field-d (p < 0.01, p = 0.015). The CTS of the buccal area was higher than in the lips.

Conclusion: The sublingual area has a homogenous distribution in TVD, FCD, FD, and SVMD. This study can be a description of the normal microvascular anatomy for future researches regarding microcirculatory assessment.
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http://dx.doi.org/10.1159/000522394DOI Listing
March 2022

Scoring the capillary leak syndrome: towards an individualized gradation of the vascular barrier injury.

Ann Intensive Care 2022 Mar 21;12(1):27. Epub 2022 Mar 21.

Department of Anesthesiology and Critical Care Medicine, Institut Lorrain du Coeur Et Des Vaisseaux, University Hospital of Nancy, Rue du Morvan, 54511, Vandoeuvre-les-Nancy, France.

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http://dx.doi.org/10.1186/s13613-022-01000-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8938581PMC
March 2022

Microcirculatory Response to Blood vs. Crystalloid Cardioplegia During Coronary Artery Bypass Grafting With Cardiopulmonary Bypass.

Front Med (Lausanne) 2021 13;8:736214. Epub 2022 Jan 13.

Department of Intensive Care, Laboratory of Translational Intensive Care, Erasmus Medical Center, Erasmus University Rotterdam, Rotterdam, Netherlands.

Blood cardioplegia attenuates cardiopulmonary bypass (CPB)-induced systemic inflammatory response in patients undergoing cardiac surgery, which may favorably influence the microvascular system in this cohort. The aim of this study was to investigate whether blood cardioplegia would offer advantages over crystalloid cardioplegia in the preservation of microcirculation in patients undergoing coronary artery bypass grafting (CABG) with CPB. In this prospective observational cohort study, 20 patients who received crystalloid ( = 10) or blood cardioplegia ( = 10) were analyzed. The microcirculatory measurements were obtained sublingually using incident dark-field imaging at five time points ranging from the induction of anesthesia (T) to discontinuation of CPB (T). In the both crystalloid [crystalloid cardioplegia group (CCG)] and blood cardioplegia [blood cardioplegia group (BCG)] groups, perfused vessel density (PVD), total vessel density (TVD), and proportion of perfused vessels (PPV) were reduced after the beginning of CPB. The observed reduction in microcirculatory parameters during CPB was only restored in patients who received blood cardioplegia and increased to baseline levels as demonstrated by the percentage changes from T to T (%Δ) in all the functional microcirculatory parameters [%ΔTVD(CCG): -10.86 ± 2.323 vs. %ΔTVD(BCG): 0.0804 ± 1.107, < 0.001; %ΔPVD(CCG): -12.91 ± 2.884 vs. %ΔPVD(BCG): 1.528 ± 1.144, < 0.001; %ΔPPV(CCG): -2.345 ± 1.049 vs. %ΔPPV(BCG): 1.482 ± 0.576, < 0.01]. Blood cardioplegia ameliorates CPB-induced microcirculatory alterations better than crystalloid cardioplegia in patients undergoing CABG, which may reflect attenuation of the systemic inflammatory response. Future investigations are needed to identify the underlying mechanisms of the beneficial effects of blood cardioplegia on microcirculation.
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http://dx.doi.org/10.3389/fmed.2021.736214DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8792788PMC
January 2022

Current practice and evolving concepts in septic shock resuscitation.

Intensive Care Med 2022 Feb 15;48(2):148-163. Epub 2021 Dec 15.

Departamento de Medicina Intensiva, Facultad de Medicina, Pontificia Universidad Católica de Chile, Santiago, Chile.

Clinical and pathophysiological understanding of septic shock has progressed exponentially in the previous decades, translating into a steady decrease in septic shock-related morbidity and mortality. Even though large randomized, controlled trials have addressed fundamental aspects of septic shock resuscitation, many questions still exist. In this review, we will describe the current standards of septic shock resuscitation, but the emphasis will be placed on evolving concepts in different domains such as clinical resuscitation targets, adequate use of fluids and vasoactive drugs, refractory shock, and the use of extracorporeal therapies. Multiple research opportunities remain open, and collaborative endeavors should be performed to fill in these gaps.
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http://dx.doi.org/10.1007/s00134-021-06595-9DOI Listing
February 2022

Endothelial dysfunction: a therapeutic target in bacterial sepsis?

Expert Opin Ther Targets 2021 09 22;25(9):733-748. Epub 2021 Oct 22.

Dept of Intensive Care Medicine, Radboud University Medical Center, Nijmegen, The Netherlands.

Introduction: Endothelial cells maintain vascular integrity, tone, and patency and have important roles in hemostasis and inflammatory responses. Although some degree of endothelial dysfunction with increased vascular permeability may be necessary to control local infection, excessive dysfunction plays a central role in the pathogenesis of sepsis-related organ dysfunction and failure as it results in dysregulated inflammation, vascular leakage, and abnormal coagulation. The vascular endothelium has thus been proposed as a potential target for therapeutic intervention in patients with sepsis.

Areas Covered: Different mechanisms underlying sepsis-related dysfunction of the vascular endothelium are discussed, including glycocalyx shedding, nitrosative stress, and coagulation factors. Potential therapeutic implications of each mechanism are mentioned.

Expert Opinion: Multiple targets to protect or restore endothelial function have been suggested, but endothelium-driven treatments remain a future potential at present. As some endothelial dysfunction and permeability may be necessary to remove infection and repair damaged tissue, targeting the endothelium may be a particular challenge. Ideally, therapies should be guided by biomarkers related to that specific pathway to ensure they are given only to patients most likely to respond. This enrichment based on biological plausibility and theragnostics will increase the likelihood of a beneficial response in individual patients and enable more personalized treatment.
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http://dx.doi.org/10.1080/14728222.2021.1988928DOI Listing
September 2021

Kidney Microcirculation as a Target for Innovative Therapies in AKI.

J Clin Med 2021 Sep 7;10(18). Epub 2021 Sep 7.

Department of Intensive Care, Laboratory of Translational Intensive Care, Erasmus MC, University Medical Center Rotterdam, 3015 GD Rotterdam, The Netherlands.

Acute kidney injury (AKI) is a serious multifactorial conditions accompanied by the loss of function and damage. The renal microcirculation plays a crucial role in maintaining the kidney's functional and structural integrity for oxygen and nutrient supply and waste product removal. However, alterations in microcirculation and oxygenation due to renal perfusion defects, hypoxia, renal tubular, and endothelial damage can result in AKI and the loss of renal function regardless of systemic hemodynamic changes. The unique structural organization of the renal microvasculature and the presence of autoregulation make it difficult to understand the mechanisms and the occurrence of AKI following disorders such as septic, hemorrhagic, or cardiogenic shock; ischemia/reperfusion; chronic heart failure; cardiorenal syndrome; and hemodilution. In this review, we describe the organization of microcirculation, autoregulation, and pathophysiological alterations leading to AKI. We then suggest innovative therapies focused on the protection of the renal microcirculation and oxygenation to prevent AKI.
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http://dx.doi.org/10.3390/jcm10184041DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8471583PMC
September 2021

Hydroxyl Ethyl Starch (HES) Preserves Intrarenal Microcirculatory Perfusion Shown by Contrast-Enhanced Ultrasound (Ceus), and Renal Function in a Severe Hemodilution Model in Pigs.

Shock 2022 03;57(3):457-466

Department of Intensive Care, Laboratory of Translational Intensive Care, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The Netherlands.

Abstract: Acute normovolemic hemodilution (ANH) is associated with low oxygen carrying capacity of blood and purposed to cause renal injury in perioperative setting. It is best accomplished in a perioperative setting by a colloid such as hydroxyl ethyl starch (HES) due its capacity to fill the vascular compartment and maintain colloidal pressure. However, alterations of intra renal microvascular perfusion, flow and its effects on renal function and damage during ANH has not been sufficiently clarified. Based on the extensive use of HES in the perioperative setting we tested the hypothesis that the use of HES during ANH is able to perfuse the kidney microcirculation adequately without causing renal dysfunction and injury in pigs. Hemodilution (n = 8) was performed by stepwise replacing blood with HES to hematocrit (Hct) levels of 20% (T1), 15% (T2), and 10% (T3). Seven control animals were investigated. Systemic and renal hemodynamics were monitored. Renal microcirculatory perfusion was visualized and quantified using contrast-enhanced ultrasound (CEUS) and laser speckle imaging (LSI). In addition, sublingual microcirculation was measured by handheld vital microscopy (HVM). Intrarenal mean transit time of ultrasound contrast agent (IRMTT-CEUS) was reduced in the renal cortex at Hct 10% in comparison to control at T3 (1.4 ± 0.6 vs. 2.2 ± 0.7 seconds, respectively, P < 0.05). Although renal function was preserved, the serum neutrophil gelatinase-associated lipocalin (NGAL) levels was higher at Hct 10% (0.033 ± 0.004 pg/μg protein) in comparison to control at T3 (0.021 ± 0.002 pg/μg protein. A mild correlation between CO and IRMTT (renal RBC velocity) (r -0.53; P = 0.001) and CO and NGAL levels (r 0.66; P = 0.001) was also found. Our results show that HES induced ANH is associated with a preserved intra renal blood volume, perfusion, and function in the clinical range of Hct (<15%). However, at severely low Hct (10%) ANH was associated with renal injury as indicated by increased NGAL levels. Changes in renal microcirculatory flow (CEUS and LSI) followed those seen in the sublingual microcirculation measured with HVM.
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http://dx.doi.org/10.1097/SHK.0000000000001862DOI Listing
March 2022

Sublingual Microcirculatory Evaluation of Extracorporeal Hemoadsorption with CytoSorb® in Abdominal Sepsis: A Case Report.

Blood Purif 2021 Sep 15:1-5. Epub 2021 Sep 15.

Department of Intensive Care Medicine, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The Netherlands.

Cytokemia is associated with microcirculatory alterations often with persistent loss of coherence between the micro- and macrocirculation, linked to organ failure and poor outcome of septic patients. Addition of a hemoadsorbant filter to an extracorporeal circuit next to conventional treatment of septic shock results in the hematological clearance of cytokines, hypothetically leading to normalization of the microcirculation and thus organ perfusion. Bedside sublingual microcirculatory assessment using handheld vital microscopy allows real-time direct visualization of the microcirculation and its response to therapy. This is demonstrated in the present case report of an 83-year-old man admitted to our intensive care unit after surgical repair of a colonic perforation for fecal soiling after a low anterior resection for a rectum carcinoma, with leakage of bowel content at the resection site. The clinical course of this patient can be described as having undergone adequate surgical treatment taking away the source of the disease, followed by optimal support including antibiotic treatment in the ICU. However, during the course of his stay in the ICU, his condition deteriorated with symptoms consistent with septic shock. Our report shows that the addition of a hemoadsorbent (CytoSorb) to the continuous renal replacement therapy circuit was associated with an improvement in the condition of our severely ill patient with abdominal sepsis. Parallel to the clinical improvement of our patient, the functional parameters of the microcirculation also showed improvement suggesting that such a noninvasive real-time evaluation of the status of the microcirculation may be a sensitive diagnostic tool to monitor the effectiveness of hemoadsorbent therapy.
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http://dx.doi.org/10.1159/000518903DOI Listing
September 2021

The Relevance of Fluid and Blood Management Using Microcirculatory Parameters in Children Undergoing Craniofacial Surgery.

J Craniofac Surg 2022 Jan-Feb 01;33(1):264-269

Department of Translational Physiology and Intensive Care Unit, University of Amsterdam and Erasmus University, Amsterdam, Rotterdam, the Netherlands.

Abstract: Perioperative management of bleeding in children can be challenging. Microvascular imaging techniques have allowed evaluating the effect of blood transfusion on the microcirculation, but little is known about these effects in children. We aimed to investigate the effects of blood management using macro- and micro-hemodynamic parameters measurement in children undergoing craniofacial surgery. This is a prospective observational repeated measurement study including fourteen children. The indications for blood transfusion were changes of hemoglobin/hematocrit (Hct) levels, the presence of signs of altered tissue perfusion and impaired microcirculation images. Total and perfused vessel densities, proportion of perfused vessels, microvascular flow index, and systemic parameters (hemoglobin, Hct, lactate, mixed venous oxygen saturation, K+, heart rate, mean arterial blood pressure) were evaluated baseline (T1), at the end of the surgical bleeding (T2) and end of the operation (T3). Four patients did not need a blood transfusion. In the other 10 patients who received a blood transfusion, capillary perfusion was higher at T3 (13[9-16]) when compared with the values of at T2 (11[8-12]) (P < 0.05) but only 6 patients reached their baseline values. Although blood transfusions increased Hct values (17 ± 2.4 [T2]-19 ± 2.8 [T3]) (P < 0.05), there was no correlation between microvascular changes and systemic hemodynamic parameters (P > 0.05). The sublingual microcirculation could change by blood transfusion but there was not any correlation between microcirculation changes, hemodynamic, and tissue perfusion parameters even with Hct values. The indication, guidance, and timing of fluid and blood therapy may be assessed by bedside microvascular analysis in combination with standard hemodynamic and biochemical monitoring for intraoperative bleeding in children.
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http://dx.doi.org/10.1097/SCS.0000000000008080DOI Listing
January 2022

Increased Hepatic Microvascular Density, Oxygenation, and VEGF in the Hypertrophic Lobe following Portal Vein Embolization in Rabbits.

Eur Surg Res 2022 15;63(1):9-18. Epub 2021 Jul 15.

Department of Surgery, Amsterdam UMC, Location AMC, University of Amsterdam, Amsterdam, The Netherlands.

Introduction: The microvascular events following portal vein embolization (PVE) are poorly understood despite the pivotal role of the microcirculation in liver regeneration and tumor progression. We aimed to assess the changes in hepatic microvascular perfusion and neo-angiogenesis after experimental PVE.

Methods: PVE of the cranial liver lobes was performed in 12 New Zealand White rabbits divided into 2 groups of permanent (P-PVE) and reversible PVE (R-PVE), respectively. Hepatobiliary scintigraphy and CT were used to evaluate hepatic function and volume. Hepatic microcirculation was assessed using a handheld vital microscope (Cytocam) to measure microvascular density (total vessel density; TVD) before PVE, right after PVE, and 20 min after PVE, as well as at 14 days (D14 post-PVE) and 35 days (D35 post-PVE). Additionally, on D35, microvascular PO2 and liver parenchymal VEGF were assessed.

Results: Eleven rabbits were included after PVE (R-PVE, n = 5; P-PVE, n = 6). TVD in the nonembo-lized (hypertrophic) lobes was higher than in the embolized (atrophic) lobes of the P-PVE group at D35 post-PVE (36.7 ± 7.2 vs. 23.4 ± 4.9 mm/mm2; p < 0.05). In the R-PVE group, TVD in the nonembolized lobes was not increased at D35. Function and volume were increased in the nonembolized lobes of the P-PVE group compared to the embolized lobes, but not in the R-PVE group. Likewise, the mmicrovascular PO2 and VEGF staining rate were higher in the nonembolized lobes of the P-PVE group at D35 post-PVE.

Discussion/conclusion: Successful volumetric and functional hypertrophy of the nonembolized lobe was accompanied by microvascular alterations featuring increased neo-angiogenesis, microvascular density, and microvascular oxygen pressure following P-PVE.
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http://dx.doi.org/10.1159/000517025DOI Listing
March 2022

Cardio-Pulmonary-Renal Consequences of Severe COVID-19.

Cardiorenal Med 2021 3;11(3):133-139. Epub 2021 Jun 3.

Department of Cardiology, Unit Heart Failure, Heart Transplantation & Mechanical Circulatory Support, Thorax Center, Rotterdam, The Netherlands.

Severe acute respiratory syndrome coronavirus 2 has rapidly spread worldwide and resulted in the coronavirus disease 2019 (COVID-19) pandemic. The disease raised an unprecedented demand for intensive care support due to severe pulmonary dysfunction and multiorgan failure. Although the pulmonary system is the potential target of the COVID-19, recent reports have demonstrated that COVID-19 profoundly influences the cardiovascular system and the kidneys. Research studies on cadavers have shown that direct heart and kidney injury can be frequently seen in patients deceased due to COVID-19 infection. On the other hand, functional or structural dysfunction of the heart may deteriorate the renal function and vice versa. This concept is already known as the cardiorenal syndrome and may play a role in COVID-19. Proactive monitoring of micro- and macrohemodynamics could allow prompt correction of circulatory dysfunction and can be of pivotal importance in the prevention of acute kidney injury. Moreover, type and amount of fluid therapy and vasoactive drug support could help manage these patients either with or without mechanical ventilator support. This brief review outlines the current evidence regarding the COVID-19-related renal and cardiorenal complications and discusses potential hemodynamic management strategies.
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http://dx.doi.org/10.1159/000516740DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8247817PMC
July 2021

Veno-arterial thrombosis and microcirculation imaging in a patient with COVID-19.

Respir Med Case Rep 2021 11;33:101428. Epub 2021 May 11.

Dept. of Intensive Care, Haga Teaching Hospital, The Hague, the Netherlands.

The Coronavirus pandemic has brought new challenges in intensive care medicine. Understanding of the pathophysiology of the vascular complications of SARS-CoV-2 infection could bring new resuscitation and therapeutic options. In this case report, we present a patient with COVID-19 pneumonia, who was admitted to our ICU and treated with high-flow nasal cannula, dexamethasone, remdesivir and high-dose prophylactic low molecular weight heparin. During ICU admission, substantial venous and arterial thrombosis developed. Meanwhile the microcirculation showed more than double amount of organ perfusion with very high total vessel density. We hypothesize that this might be a compensatory mechanism for the generalized prothrombic state in which the microcirculation increases the oxygen extraction capacity preventing multi-organ failure.
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http://dx.doi.org/10.1016/j.rmcr.2021.101428DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8110328PMC
May 2021

Effect of norepinephrine challenge on cardiovascular determinants assessed using a mathematical model in septic shock: a physiological study.

Ann Transl Med 2021 Apr;9(7):561

Department of Intensive Care, Erasmus MC University Hospital, Rotterdam, The Netherlands.

Background: The present study investigated the cardiovascular determinants of cardiac output (CO), mean systemic filling pressure analogue (Pmsa) derived by Geoffrey Parkin, efficiency of heart (Eh) and related parameters to a norepinephrine (NE) challenge [an increase of 10 mmHg mean arterial pressure (MAP) by NE] in septic shock patients using of a mathematical model.

Methods: Twenty-seven septic shock patients with pulse index continuous cardiac output (PiCCO) monitoring were enrolled. These patients required NE to maintain an individualized MAP for organ perfusion after early fluid resuscitation based on their clinical condition. NE was decreased to obtain a decrease of 10 mmHg from base MAP (MAP), and the NE doses were adjusted to return MAP to baseline (MAP) and produce an increase of 10 mmHg from MAP (MAP). Two NE challenge episodes were analyzed for each patient: from MAP to MAP and from MAP to MAP. The Pmsa, pressure gradient for venous return (PG), and Eh (PGvr relative to Pmsa) were estimated using a mathematical model for the three MAP levels (MAP, MAP and MAP).

Results: A total of 54 episodes of NE challenges were obtained in 27 patients. Significant and consistent increases were observed in the central venous pressure (CVP), Pmsa, and PGvr in response during the NE titration. ΔCO negatively and significantly correlated with ΔCVP (r=-0.722, P<0.0001), ΔPmsa (r=-0.549, P<0.0001), ΔResistance of venous return (Rvr) (r=-0.597, P<0.0001), and ΔResistance of systemic vascular beds (Rsys) (r=-0.597, P<0.0001). Episodes of decreasing CO/Eh were associated with a higher ΔCVP than the CO/Eh-increasing episodes. The area under the curve (AUC) of ΔCVP to predict decreased CO by the incremental NE was 0.86, and the AUC of ΔCVP to predict decreased Eh was 0.94. A cutoff of ΔCVP >1.5 mmHg for detecting decreased CO resulted in a sensitivity of 75% and a specificity of 94.1%. A cutoff of ΔCVP >1.5 mmHg for detecting decreased Eh resulted in a sensitivity of 64.3% and a specificity of 100%.

Conclusions: There were a highly divergent response in Eh and CO to afterload challenge episodes of an NE-induced 10mmHg increase in MAP. An increase in CVP may be an early alarm to identify the reduction in CO/Eh during an NE-induced increase of MAP.
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http://dx.doi.org/10.21037/atm-20-6686DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105783PMC
April 2021

Microcirculatory Response to Changes in Venoarterial Extracorporeal Membrane Oxygenation Pump Flow: A Prospective Observational Study.

Front Med (Lausanne) 2021 7;8:649263. Epub 2021 Apr 7.

Department of Anesthesiology, National Taiwan University Hospital, College of Medicine, National Taiwan University, Taipei, Taiwan.

Venoarterial extracorporeal membrane oxygenation (VA-ECMO) pump flow is crucial for maintaining organ perfusion in patients with cardiogenic shock, but VA-ECMO pump flow optimization remains as a clinical challenge. This study aimed to investigate the response of sublingual microcirculation to changes in VA-ECMO pump flow. Sublingual microcirculation was measured before and after changing VA-ECMO pump flow according to the treatment plan of ECMO team within 24 h and at 24-48 h after VA-ECMO placement. In clinical events of increasing VA-ECMO pump flow, those events with increased perfused vessel density (PVD) were grouped into group A, and the others were grouped into group B. In clinical events of decreasing VA-ECMO pump flow, those events with increased PVD were grouped into group C, and the others were grouped into group D. Increased PVD was observed in 60% (95% CI, 38.5-81.5%) of the events with increasing VA-ECMO pump flow. The probability of increasing PVD after increasing VA-ECMO pump flow were higher in the events with a PVD < 15 mm/mm at baseline than those with a PVD ≥ 15 mm/mm [100% (95% CI, 54.1-100%) vs. 42.9% (95% CI, 17.7-71.1%), = 0.042]. Other microcirculatory and hemodynamic parameters at baseline did not differ significantly between group A and B or between group C and D. This study revealed contradictory and non-contradictory responses of sublingual microcirculation to changes in VA-ECMO pump flow. Tandem measurements of microcirculation before and after changing VA-ECMO pump flow may help to ensure a good microcirculation.
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http://dx.doi.org/10.3389/fmed.2021.649263DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8058194PMC
April 2021

Corrections to "Microbubble Composition and Preparation for High-Frequency Contrast-Enhanced Ultrasound Imaging: In Vitro and In Vivo Evaluation".

IEEE Trans Ultrason Ferroelectr Freq Control 2021 06 25;68(6):2321. Epub 2021 May 25.

In the above article [1], the authors regret that there was a mistake in calculating the mol% of the microbubble coating composition used. For all experiments, the unit in mg/mL was utilized and the conversion mistake only came when converting to mol% in order to define the ratio between the coating formulation components. The correct molecular weight of PEG-40 stearate is 2046.54 g/mol [2], [3], not 328.53 g/mol. On page 556, Table I should read as shown here.
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http://dx.doi.org/10.1109/TUFFC.2021.3067599DOI Listing
June 2021

Case Report: Sublingual Microcirculatory Alterations in a Covid-19 Patient With Subcutaneous Emphysema, Venous Thrombosis, and Pneumomediastinum.

Front Med (Lausanne) 2020 28;7:624695. Epub 2021 Jan 28.

Department of Intensive Care, Haga Teaching Hospital, The Hague, Netherlands.

The Corona virus disease 2019 (Covid-19) has brought a wide range of challenges in intensive care medicine. Understanding of the pathophysiology of Covid-19 relies on interpreting of its impact on the vascular, particularly microcirculatory system. Herein we report on the first use of the latest generation hand-held vital microscope to evaluate the sublingual microcirculation in a Covid-19 patient with subcutaneous emphysema, venous thrombosis and pneumomediastinum. Remarkably, microcirculatory parameters of the patient were increased during the exacerbation period, which is not a usual finding in critically ill patients mostly presenting with a loss of hemodynamic coherence. In contrast, recovery from the disease led to a subsequent amelioration of these parameters. This report clearly shows the importance of microcirculatory monitoring for evaluating the course and the adequacy of therapy in Covid-19 patients.
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http://dx.doi.org/10.3389/fmed.2020.624695DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7876339PMC
January 2021

Noninvasive, in vivo assessment of the cervical microcirculation using incident dark field imaging.

Microvasc Res 2021 05 9;135:104145. Epub 2021 Feb 9.

Amsterdam UMC, University of Amsterdam, Department of Obstetrics and Gynaecology, Amsterdam Reproduction & Development Research Institute, Meibergdreef 9, 1105 AZ Amsterdam, the Netherlands; Bergman Clinics, Department of Gynaecology, Bergman Vrouwenzorg, Nijenburg 152, 1081 GG Amsterdam, the Netherlands.

Aim: This study evaluates the feasibility of handheld vital microscopy for noninvasive, objective assessment of the microcirculation of the human uterine cervix. We qualitatively and quantitatively describe the microcirculation in healthy subjects in order to provide a basis for its application in cervical pathology.

Methods: Incident dark field imaging was used to image the microcirculation in four quadrants of the uterine ectocervix in ten healthy participants. If the squamocolumnar junction was visible, measurements were repeated on the endocervical columnar epithelium as well. Image acquisition time was recorded and participants scored the experienced level of discomfort. Angioarchitecture was classified according to Weber's classification. Quantitative parameters included capillary density (CD), total and perfused vessel density (TVD, PVD), proportion of perfused vessels (PPV) and microvascular flow index (MFI).

Results: Image acquisition was easy, fast and well tolerated. Angioarchitecture was characterized by two distinctive and organized patterns; capillary loops underneath the squamous epithelium of the ectocervix and vascular networks underneath the columnar epithelium. In the image sequences containing capillary loops, mean CD was 33.2 cpll/mm (95% CI 28.2-38.2 cpll/mm). In the image sequences with vascular networks, mean TVD was 12.5 mm/mm (95% CI 11.2-13.77 mm/mm), mean PVD was 12.2 (95% CI 11.0-13.5 mm/mm), MFI was 3 and PPV was 100%.

Conclusions: Incident dark field imaging allows for noninvasive, real time visualization and objective evaluation and quantification of the microcirculation of the uterine cervix. The organized vascular patterns and optimal perfusion observed in healthy subjects allow for comparison with cervical pathology, for example in patients with cervical dysplasia or cervical cancer.
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http://dx.doi.org/10.1016/j.mvr.2021.104145DOI Listing
May 2021

Capillary Leukocytes, Microaggregates, and the Response to Hypoxemia in the Microcirculation of Coronavirus Disease 2019 Patients.

Crit Care Med 2021 04;49(4):661-670

Department of Intensive Care, Erasmus MC, University Medical Center, Rotterdam, The Netherlands.

Objectives: In this study, we hypothesized that coronavirus disease 2019 patients exhibit sublingual microcirculatory alterations caused by inflammation, coagulopathy, and hypoxemia.

Design: Multicenter case-controlled study.

Setting: Two ICUs in The Netherlands and one in Switzerland.

Patients: Thirty-four critically ill coronavirus disease 2019 patients were compared with 33 healthy volunteers.

Interventions: None.

Measurements And Main Results: The microcirculatory parameters quantified included total vessel density (mm × mm-2), functional capillary density (mm × mm-2), proportion of perfused vessels (%), capillary hematocrit (%), the ratio of capillary hematocrit to systemic hematocrit, and capillary RBC velocity (μm × s-1). The number of leukocytes in capillary-postcapillary venule units per 4-second image sequence (4 s-1) and capillary RBC microaggregates (4 s-1) was measured. In comparison with healthy volunteers, the microcirculation of coronavirus disease 2019 patients showed increases in total vessel density (22.8 ± sd 5.1 vs 19.9 ± 3.3; p < 0.0001) and functional capillary density (22.2 ± 4.8 vs 18.8 ± 3.1; p < 0.002), proportion of perfused vessel (97.6 ± 2.1 vs 94.6 ± 6.5; p < 0.01), RBC velocity (362 ± 48 vs 306 ± 53; p < 0.0001), capillary hematocrit (5.3 ± 1.3 vs 4.7 ± 0.8; p < 0.01), and capillary-hematocrit-to-systemic-hematocrit ratio (0.18 ± 0.0 vs 0.11 ± 0.0; p < 0.0001). These effects were present in coronavirus disease 2019 patients with Sequential Organ Failure Assessment scores less than 10 but not in patients with Sequential Organ Failure Assessment scores greater than or equal to 10. The numbers of leukocytes (17.6 ± 6.7 vs 5.2 ± 2.3; p < 0.0001) and RBC microaggregates (0.90 ± 1.12 vs 0.06 ± 0.24; p < 0.0001) was higher in the microcirculation of the coronavirus disease 2019 patients. Receiver-operating-characteristics analysis of the microcirculatory parameters identified the number of microcirculatory leukocytes and the capillary-hematocrit-to-systemic-hematocrit ratio as the most sensitive parameters distinguishing coronavirus disease 2019 patients from healthy volunteers.

Conclusions: The response of the microcirculation to coronavirus disease 2019-induced hypoxemia seems to be to increase its oxygen-extraction capacity by increasing RBC availability. Inflammation and hypercoagulation are apparent in the microcirculation by increased numbers of leukocytes and RBC microaggregates.
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http://dx.doi.org/10.1097/CCM.0000000000004862DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7963442PMC
April 2021

Improved Survival beyond 28 Days up to 1 Year after CytoSorb Treatment for Refractory Septic Shock: A Propensity-Weighted Retrospective Survival Analysis.

Blood Purif 2021 22;50(4-5):539-545. Epub 2020 Dec 22.

Department of Intensive Care Medicine, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The Netherlands.

Background And Aims: It is currently unknown whether CytoSorb treatment for septic shock improves long-term survival beyond 28 days from intensive care unit (ICU) admission and which factors determine outcome.

Methods: This was a long-term follow-up retrospective analysis of patients with septic shock who were treated with continuous renal replacement therapy (CRRT) + CytoSorb (n = 67) or CRRT alone (n = 49). These patients were previously analyzed for 28-day mortality. The primary outcome was the time to long-term all-cause mortality. Factors associated with time to event were analyzed both weighted by stabilized inverse probability of treatment weights (sIPTW) as well as unweighted stratified by therapy received.

Results: The median follow-up for the total cohort was 30 days (interquartile range [IQR]: 5-334, maximum 1,059 days) after ICU admission and 333 days (IQR: 170-583) for those who survived beyond 28 days (n = 59). Survival beyond 28 days was sustained up to 1 year after ICU admission for both treatment regimens: 80% (standard error [SE] 7%) vs. 87% (SE 7%), for CytoSorb vs. CRRT, respectively, p = 0.853. By sIPTW, CytoSorb was significantly associated with long-term outcome compared to CRRT (adjusted hazard ratio [aHR] 0.59, 95% confidence interval [CI] 0.37-0.93, p = 0.025). Independent factors associated with long-term outcome in CytoSorb-treated patients were baseline log10 lactate levels (aHR 5.1, p = 0.002), age in the presence of comorbidity (aHR 2.60, p = 0.013), and presence of abdominal sepsis (aHR 0.34, p = 0.004). A lactate level above 6.0 mmol/L at the start of CytoSorb therapy had a positive predictive value of 79% for mortality (p = 0.013).

Conclusions: Survival is achieved with CytoSorb and CRRT for patients with septic shock beyond 28 days from ICU admission and may be improved for CytoSorb treatment. Lactate levels above 6.0 mmol/L at the start of CytoSorb therapy are predictive of worse outcome with high specificity and positive predictive value.
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http://dx.doi.org/10.1159/000512309DOI Listing
January 2022

The effect of blood transfusion on sublingual microcirculation in critically ill patients: A scoping review.

Microcirculation 2021 04 9;28(3):e12666. Epub 2020 Nov 9.

Department of Critical Care Medicine, Peking Union Medical College Hospital, Beijing, China.

Purpose: To investigate the effects of red blood cell (RBC) transfusion on sublingual microcirculation in critically ill patients.

Methods: Systematic strategy was conducted to search studies that measured sublingual microcirculation before and after transfusion in critically ill patients. This review was reported according to the Preferred Reporting Items for Systematic Review and Meta-Analyses Scoping Review Extension.

Results: The literature search yielded 114 articles. A total of 11 studies met the inclusion criteria. Observational evidence showed diffusive capacity of the microcirculation significantly improved in intraoperative and anemic hematologic patients after transfusion, while the convective parameters significantly improved in traumatic patients. RBC transfusion improved both diffusive and convective microcirculatory parameters in hypovolemic hemorrhagic shock patients. Most of the studies enrolled septic patients showed no microcirculatory improvements after transfusion. The positive effects of the leukoreduction were insufficiently supported. The effects of the storage time of the RBCs were not conclusive. The majority of the evidence supported a negative correlation between baseline proportion of perfused vessels (PPV) and changes in PPV.

Conclusions: This scoping review has catalogued evidence that RBC transfusion differently improves sublingual microcirculation in different populations. The existing evidence is not sufficient to conclude the effects of the leukoreduction and storage time of RBCs.
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http://dx.doi.org/10.1111/micc.12666DOI Listing
April 2021

Detection of inadequate anastomotic perfusion with handheld vital microscopy in two patients during colorectal surgery.

Clin J Gastroenterol 2021 Feb 21;14(1):141-145. Epub 2020 Sep 21.

Department of Surgery, St. Antonius Hospital, Nieuwegein, The Netherlands.

Introduction: Anastomotic leakage is one of the most feared complications after gastrointestinal surgery. Assessment of anastomotic viability during surgery remains challenging. Sufficient bowel tissue perfusion is a requisite for anastomotic healing. Handheld vital microscopy (HVM) is a non-invasive technique that can directly visualize the intestinal microcirculation during surgery.

Presentation Of Two Cases: Two patients underwent elective laparoscopic colorectal surgery. During surgery HVM was used to assess bowel perfusion prior to creation of a primary anastomosis. Although the bowel macroscopically appeared to be well perfused, HVM showed a severely compromised microcirculation. The colon was re-internalized and during the following minutes cyanosis of the bowel occurred which was visually determined by the surgeon. After dissection towards cranially, a new site for the primary anastomosis was chosen. The postoperative period was uncomplicated.

Discussion: Sufficient bowel tissue perfusion is often mentioned as key in the pathophysiology of anastomotic leakage. HVM is a technique that could potentially aid surgeons in the assessment of microcirculatory perfusion of the bowel during surgery.

Conclusion: We report two cases undergoing colorectal surgery in which HVM showed merit in detecting compromised bowel perfusion before creation of a primary anastomosis.
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http://dx.doi.org/10.1007/s12328-020-01235-zDOI Listing
February 2021

Automated Algorithm Analysis of Sublingual Microcirculation in an International Multicentral Database Identifies Alterations Associated With Disease and Mechanism of Resuscitation.

Crit Care Med 2020 10;48(10):e864-e875

Department of Intensive Care, Erasmus MC, University Medical Center, Rotterdam, The Netherlands.

Objectives: Reliable automated handheld vital microscopy image sequence analysis and the identification of disease states and effects of therapy are prerequisites for the routine use of quantitative sublingual microcirculation measurements at the point-of-care. The present study aimed to clinically validate the recently introduced MicroTools software in a large multicentral database of perioperative and critically ill patients and to use this automatic algorithm to data-mine and identify the sublingual microcirculatory variable changes in response to disease and therapy.

Design: Retrospective algorithm-based image analysis and data-mining within a large international database of sublingual capillary microscopy. Algorithm-based analysis was compared with manual analysis for validation. Thereafter, MicroTools was used to identify the functional microcirculatory alterations associated with disease conditions and identify therapeutic options for recruiting functional microcirculatory variables.

Setting: Ten perioperative/ICU/volunteer studies in six international teaching hospitals.

Patients: The database encompass 267 adult and pediatric patients undergoing surgery, treatment for sepsis, and heart failure in the ICU and healthy volunteers.

Interventions: Perioperative and ICU standard of care.

Measurements And Main Results: One thousand five hundred twenty-five handheld vital microscopy image sequences containing 149,257 microscopy images were analyzed. 3.89 × 10 RBC positions were tracked by the algorithm in real time, and offline manual analysis was performed. Good correlation and trending ability were found between manual and automatic total and functional capillary density (r = 0.6-0.8; p < 0.0001). RBC tracking within the database demonstrated changes in functional capillary density and/or RBC velocity in septic shock, heart failure, hypovolemia, obstructive shock, and hemodilution and thus detected the presence of a disease condition. Therapies recruiting the microcirculatory diffusion and convection capacity associated with systemic vasodilation and an increase in cardiac output were separately identified.

Conclusions: Algorithm-based analysis of the sublingual microcirculation closely matched manual analysis across a broad spectrum of populations. It successfully identified a methodology to quantify microcirculatory alterations associated with disease and the success of capillary recruitment, improving point-of-care application of microcirculatory-targeted resuscitation procedures.
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http://dx.doi.org/10.1097/CCM.0000000000004491DOI Listing
October 2020

Novel non-invasive imaging method for baseline risk stratification in cardiac surgery patients.

BMJ Case Rep 2020 Sep 8;13(9). Epub 2020 Sep 8.

Department of Cardiothoracic Surgery, Amsterdam UMC-AMC Campus, Amsterdam, The Netherlands

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http://dx.doi.org/10.1136/bcr-2020-234950DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7481092PMC
September 2020

Effects of Hemoadsorption with Cytosorb during Severe Rhabdomyolysis: Reply to the Letter to the Editor of Daum and Colleagues.

Blood Purif 2021 3;50(2):273-274. Epub 2020 Sep 3.

Department of Intensive Care, Erasmus Medical Centre, University Medical Center, Rotterdam, The Netherlands.

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http://dx.doi.org/10.1159/000509898DOI Listing
July 2021

Hemodilution causes glycocalyx shedding without affecting vascular endothelial barrier permeability in rats.

J Clin Transl Res 2020 Jun 12;5(5):243-252. Epub 2020 May 12.

Department of Adult Intensive Care, Erasmus MC, University Medical Center Rotterdam, Rotterdam, The Netherlands.

Background: The consequences of acute normovolemic hemodilution (ANH) following different types of fluids on the different components of the glycocalyx and on vascular barrier permeability (VBP) remain unknown.

Aim: The aim of the study was to investigate whether the microcirculatory disruption and glycocalyx shedding induced by ANH alters VBP and whether this is affected by the composition and volume of the resuscitation fluid.

Materials And Methods: Anesthetized Wistar albino rats (n=24) underwent stepwise ANH at hematocrit levels of 35%, 25%, 20%, and 15% induced by the exchange of blood with 6% balanced hydroxyethyl starch (1:1), balanced crystalloid (1:3), and normal saline (NS) (1:3). Glycocalyx-shed products were measured at each level of hemodilution. VBP was reflected in the decay of fluorescence dyes of different molecular size and their plasma retention ratios. Edema was assessed by measuring organ water content and muscle microcirculation by hand-held videomicroscopy.

Results: NS caused increased degradation of heparan sulfate and hyaluronan compared with the control group (=0.003, =0.004, respectively). Neither VBP nor tissue edema was affected by the fluid used. The total and perfused vessel densities within the microcirculation of muscle tissue decreased at hematocrit 15% in the balanced crystalloid (=0.02) and NS groups only (<0.0001, =0.0003, respectively) compared with baseline.

Conclusions: Balanced colloid solution preserved the glycocalyx layer better than balanced and unbalanced crystalloid solutions while maintaining the microcirculatory function associated with an improved total intravascular volume. Among the fluids tested, NS caused the most microcirculatory alterations. While ANH caused the degradation of glycocalyx components regardless of fluid, it did not disrupt the vascular barrier as indicated by macromolecular leakage.

Relevance For Patients: The results of this study provide insight into the choice of fluid for optimal perioperative fluid management and the consequences of fluid type on the vascular barrier, glycocalyx, and microcirculation.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7453805PMC
June 2020

Intraoperative Imaging Techniques to Visualize Hepatic (Micro)Perfusion: An Overview.

Eur Surg Res 2020 13;61(1):2-13. Epub 2020 Jul 13.

Department of Surgery, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands.

The microcirculation plays a crucial role in the distribution of perfusion to organs. Studies have shown that microcirculatory dysfunction is an independent predictor of morbidity and mortality. Hence, assessment of liver perfusion offers valuable information on the (patho)physiological state of the liver. The current review explores techniques in perfusion imaging that can be used intraoperatively. Available modalities include dynamic contrast-enhanced ultrasound, handheld vital microscopes, indocyanine green fluorescence angiography, and laser contrast speckle imaging. Dynamic contrast-enhanced ultrasound relays information on deep tissue perfusion and is a commonly used technique to assess tumor perfusion. Handheld vital microscopes provide direct visualization of the sinusoidal architectural structure of the liver, which is a unique feature of this technique. Intraoperative fluorescence imaging uses indocyanine green, a dye that is administered intravenously to visualize microvascular perfusion when excited using near-infrared light. Laser speckle contrast imaging produces non-contact large surface-based tissue perfusion imaging free from movement- or pressure-related artefacts. In this review, we discuss the intrinsic advantages and disadvantages of these techniques and their clinical and/or scientific applications.
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http://dx.doi.org/10.1159/000508348DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7592948PMC
July 2021

Assessment of sublingual microcirculation in critically ill patients: consensus and debate.

Ann Transl Med 2020 Jun;8(12):793

Department of Intensive Care Med, Laboratory of Translational Intensive Care Med, Erasmus MC, University Medical Center, Rotterdam, The Netherlands.

The main concern in shock and resuscitation is whether the microcirculation can carry adequate oxygen to the tissues and remove waste. Identification of an intact coherence between macro- and microcirculation during states of shock and resuscitation shows a functioning regulatory mechanism. However, loss of hemodynamic coherence between the macro and microcirculation can be encountered frequently in sepsis, cardiogenic shock, or any hemodynamically compromised patient. This loss of hemodynamic coherence results in an improvement in macrohemodynamic parameters following resuscitation without a parallel improvement in microcirculation resulting in tissue hypoxia and tissue compromise. Hand-held vital microscopes (HVMs) can visualize the microcirculation and help to diagnose the nature of microcirculatory shock. Although treatment with the sole aim of recruiting the microcirculation is as yet not realized, interventions can be tailored to the needs of the patient while monitoring sublingual microcirculation. With the help of the newly introduced software, called MicroTools, we believe sublingual microcirculation monitoring and diagnosis will be an essential point-of-care tool in managing shock patients.
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http://dx.doi.org/10.21037/atm.2020.03.222DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7333125PMC
June 2020

Interpatient heterogeneity in hepatic microvascular blood flow during vascular inflow occlusion (Pringle manoeuvre).

Hepatobiliary Surg Nutr 2020 Jun;9(3):271-283

Department of Surgery, Amsterdam UMC, Location Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.

Background: Vascular inflow occlusion (VIO) during liver resections (Pringle manoeuvre) can be applied to reduce blood loss, however may at the same time, give rise to ischemia-reperfusion injury (IRI). The aim of this study was to assess the characteristics of hepatic microvascular perfusion during VIO in patients undergoing major liver resection.

Methods: Assessment of hepatic microcirculation was performed using a handheld vital microscope (HVM) at the beginning of surgery, end of VIO (20 minutes) and during reperfusion after the termination of VIO. The microcirculatory parameters assessed were: functional capillary density (FCD), microvascular flow index (MFI) and sinusoidal diameter (SinD).

Results: A total of 15 patients underwent VIO; 8 patients showed hepatic microvascular perfusion despite VIO (partial responders) and 7 patients showed complete cessation of hepatic microvascular perfusion (full responders). Functional microvascular parameters and blood flow levels were significantly higher in the partial responders when compared to the full responders during VIO (FCD: 0.84±0.88 . 0.00±0.00 mm/mm, P<0.03, respectively, and MFI: 0.69-0.22 . 0.00±0.00, P<0.01, respectively).

Conclusions: An interpatient heterogeneous response in hepatic microvascular blood flow was observed upon VIO. This may explain why clinical strategies to protect the liver against IRI lacked consistency.
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http://dx.doi.org/10.21037/hbsn.2020.02.04DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7262621PMC
June 2020

Intravenous fluid therapy in the perioperative and critical care setting: Executive summary of the International Fluid Academy (IFA).

Ann Intensive Care 2020 May 24;10(1):64. Epub 2020 May 24.

Department of Intensive Care Medicine, Ziekenhuis Netwerk Antwerpen, ZNA Stuivenberg, Antwerp, Belgium.

Intravenous fluid administration should be considered as any other pharmacological prescription. There are three main indications: resuscitation, replacement, and maintenance. Moreover, the impact of fluid administration as drug diluent or to preserve catheter patency, i.e., fluid creep, should also be considered. As for antibiotics, intravenous fluid administration should follow the four Ds: drug, dosing, duration, de-escalation. Among crystalloids, balanced solutions limit acid-base alterations and chloride load and should be preferred, as this likely prevents renal dysfunction. Among colloids, albumin, the only available natural colloid, may have beneficial effects. The last decade has seen growing interest in the potential harms related to fluid overloading. In the perioperative setting, appropriate fluid management that maintains adequate organ perfusion while limiting fluid administration should represent the standard of care. Protocols including a restrictive continuous fluid administration alongside bolus administration to achieve hemodynamic targets have been proposed. A similar approach should be considered also for critically ill patients, in whom increased endothelial permeability makes this strategy more relevant. Active de-escalation protocols may be necessary in a later phase. The R.O.S.E. conceptual model (Resuscitation, Optimization, Stabilization, Evacuation) summarizes accurately a dynamic approach to fluid therapy, maximizing benefits and minimizing harms. Even in specific categories of critically ill patients, i.e., with trauma or burns, fluid therapy should be carefully applied, considering the importance of their specific aims; maintaining peripheral oxygen delivery, while avoiding the consequences of fluid overload.
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http://dx.doi.org/10.1186/s13613-020-00679-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7245999PMC
May 2020
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