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restoring macro-hemodynamics, mortality remains Introduction high [8, 9]. Some studies even report that up to 45% of To date, even if there is no precise uniform definition of patients dying from CS have a normalized cardiac index cardiogenic shock (CS), it is generally considered as a (CI) (i.e., > 2.2 L/min/m ), indicating that optimization state of tissue and end-organ hypoperfusion caused by of macrocirculatory parameters alone is not enough an ineffective cardiac output (CO) unable to deliver suf - [10]. This may be in part explained by organ-perfusion ficient oxygen to organs and peripheral tissues fulfilling disorders that extend beyond the macrocirculation and metabolic demands, assumed that intravascular volume subsequently drive multiple organ failures. The state is adequate [1, 2]. This inadequate end-organ perfusion where main macrocirculation parameters such as BP associated with microcirculatory dysfunction and multi- and CI are restored, while microcirculation parameters ple organ failure is included in all current definitions of are not, is called “loss of hemodynamic coherence”. CS as “signs of poor peripheral tissue perfusion”, such as Indeed, in CS, vascular regulation and compensatory cold extremities, mottling, elevated capillary refill time mechanisms needed to sustain hemodynamic coher- (CRT), altered mental status, oliguria or elevated arte- ence appear to be lost in most cases, resulting in rial lactate levels [3]. However, only recently have stud- regional microcirculation remaining in shock. This ies attempted to better characterize the microcirculatory so-called “loss of hemodynamic coherence” between dysfunction in CS [4]. macrohemodynamic and microhemodynamic param- Many studies showed that CS not only involves sys- eters evidences that microvascular perfusion is one of temic macrocirculation abnormalities, such as blood the major determinants of clinical outcome in CS [11, pressure (BP), left ventricular ejection fraction (LVEF), 12]. Microcirculation is a complex system regulating or CO [5], but also significant abnormalities of the sys - the balance between tissues’ oxygen consumption and temic microcirculation [6, 7]. Indeed, despite progress in the management of CS, in particular by promptly M erdji et al. Annals of Intensive Care (2023) 13:38 Page 3 of 15 Fig. 1 Microcirculation structure and function. The organ vasculature system has been anatomically and functionally subclassified into macro and microcirculation. Macrocirculation is constituted by conduction arteries (such as the aorta) before entering the resistance arteries (such as the mesenteric arteries) with the main purpose of transporting blood. Microcirculation is composed of pre-arterioles and arterioles regulating blood flow, leading to capillaries allowing the exchange of gases, nutrients, hormones, and other molecules delivery (Fig. 1) [13]. So far, microcirculatory disorders especially during acute myocardial infarction (AMI) have been widely explored in the context of intensive which is beyond the scope of this review [18]. care medicine, mostly in septic shock, showing highly heterogeneous alterations with clear evidence of arte- Epidemiology of cardiogenic shock riolar–venular shunting [14, 15] in different tissues Cardiogenic shock incidence has been constantly including the lungs, the kidneys, the liver, the gas- increasing for several years in United States of America trointestinal tract and the brain [16]. Further studies and Europe, now accounting for almost 8% of admis- are, therefore, still necessary focusing exclusively on sions in ICU [19]. Although Harrison introduced CS as microcirculation dysfunction in CS and its specificities a specific entity in 1939 and differentiated it from other [17]. Despite the paucity of clinical data on microcir- forms of shock, CS remains nowadays one of the great- culation-enhancing therapies to date, a better under- est challenges in cardiology and intensive care medicine. standing of these dysfunctions might help improve CS Cardiogenic shock is the most severe manifestation of management in the future. Thus, this narrative review AHF, accounting for < 5% of acute heart failure (AHF) article will focus on systemic microcirculatory dys- cases in the western world [20]. Compared to AHF, CS function in CS and its specificities. This review will not has tenfold higher in-hospital mortality, remaining > 40% discuss specific coronary microcirculation alteration, despite recent advances [21, 22]. Unlike CS, patients with AHF do not exhibit prolonged hypotension with systolic blood pressure (SBP) < 90 mmHg and do not require vasopressors to raise SBP > 90 mmHg in the absence Merdji et al. Annals of Intensive Care (2023) 13:38 Page 4 of 15 Table 1 Main differences between acute heart failure and cardiogenic shock Acute heart failure Cardiogenic shock Onset • Days (e.g., acute decompensated heart failure) • Hours • Hours (e.g., acute pulmonary oedema) Blood pressure • SBP > 90 mmHg • Life-threatening hypotension with SBP < 90 mmHg or MAP < 60 mmHg • BP may be initially preserved by compensatory vasoconstriction 2 2 Cardiac index (CI) • CI > 2.2 L/min/m usually • Low CI ≤ 2.2 L/min/m Hypoperfusion and organ dysfunction • Sometimes • Always Main clinical presentations • Wet-warm (∼70%) • Wet-cold (∼65%) • Wet-cold (∼20%) • Dry-cold (∼30%) Need for vasopressors/inotropes to achieve and maintain • No • Yes a target SBP > 90 mmHg or MAP ≥ 65 mmHg Arterial lactate • < 2 mmol/L usually • ≥ 2 mmol/L pH level • Normal pH usually • Metabolic acidosis Consider temporary MCS • Rarely (e.g., “protected PCI” with Impella) • Sometimes This main clinical presentation is based on bedside evaluation and categorization by clinical signs of congestion (‘wet’ vs. ‘dry’ if present vs. absent) and hypoperfusion (‘cold’ vs. ‘warm’ if present vs. absent) CI cardiac index, MAP mean arterial pressure, MCS mechanical circulatory support, SBP systolic blood pressure of hypovolemia (Table 1) [23]. In contrast to AHF, CS in the microcirculation to the tissues. First, capillary mainly shows signs of hypoperfusion, such as increased blood flow is a complex product of arteriolar tone, driv - capillary refill time, mottling, cold periphery or clammy ing pressure, and hemorheology allowing convection skin, confusion, oliguria, and elevated serum lactate [23]. of oxygen-carrying erythrocytes (convective capacity). Indeed, studies report that CS main clinical presentations The second is capillary patency, reflected by functional are mostly wet-cold (∼65%) and dry-cold (∼30%) (“cold” capillary density. This functional capillary density rep - meaning hypoperfusion), while AHF has signs of hypop- resents the number of normally perfused capillaries in erfusion in less than 20% of the cases usually [24, 25]. a given tissue area (diffusive capacity). The performance of organs and tissues is, therefore, critically dependent on a functional microcapillary net- From heart to microcirculation via macrocirculation: work that maintains delivery of oxygen, exchanges heat, the cardiov ‑ ascular continuum and nutrients, and removes carbon dioxide and waste Once ejected by the left ventricle, the oxygenated blood products [29]. Of note, a decline in capillary density will progressively pass through conductance arter- might be one of the major causes of aging and age- ies (such as the aorta) before entering resistance arter- related diseases [30]. ies (such as mesenteric arteries) and then will reach the Under physiological conditions, blood arrives micro- microcirculation [13]. circulation through pre-arterioles (100–400 µm in diam- Microcirculation is the terminal vascular network eter) before reaching arterioles (10–50 µm in diameter), of systemic circulation consisting of microvessels with which are both surrounded by a thick, continuous layer diameters < 20 μm including arterioles, capillaries, and of smooth muscle. Contraction of the smooth muscle venules [26] (Fig. 1), Altogether, it represents the largest reduces the lumen of these microvessels and, therefore, vascular surface area in the body. This part of the cir - increases the resistance to blood flow throughout the culation is critical as it is responsible for oxygen trans- entire vascular bed, making the arteriole the major resist- fer and nutrient delivery from the erythrocytes in the ance component in the circulation and the main driver capillaries to the parenchymal cells to meet their met- of the total peripheral resistance. Smooth muscle tone in abolic demands. Microcirculation is also involved in the arterioles also regulates the amount of pressure trans- regulating blood flow and tissue perfusion in response mitted from the arteries to the veins; thus, capillary pres- to hemodynamic alterations, to tailor oxygen delivery sure decreases when the arterioles contract and increases across microvascular beds with different oxygen needs. when the arterioles dilate. In addition, microcirculation has a central role in the Further to the arterioles, the blood then enters a nar- immune system including hemostasis via mechanisms, rower vessel, the metarteriole (10–20 µm), which such as immunothrombosis [27, 28]. Two main primary is the terminal end of the arteriole surrounded by a factors ensure oxygen transport by erythrocyte flow M erdji et al. Annals of Intensive Care (2023) 13:38 Page 5 of 15 discontinuous smooth muscle layer. From the metart- a higher concentration of soluble thrombomodulin than eriole, capillaries (5–10 µm in diameter and length of AMI patients without CS, reflecting endothelial damage 5 mm), a single layer of epithelium, and a basement [39]. membrane arise and branch off. Capillary density, which Located between the bloodstream and the endothe- is an important determinant of the total surface area lium, the endothelial glycocalyx is an important available for blood–tissue exchange, varies considerably determinant of vascular homeostasis, composed of mac- from one organ to another depending on the metabolic romolecules such as proteoglycans and sialoprotein and requirement. In human tissue, the average capillary den- also organ- and vascular bed-specific [40]. The glycoca - sity is around 600 per mm , but it is higher in brain, lung, lyx is a 0.2–0.5 μm-thick gel-like layer lining the lumi- kidneys, liver, and myocardium (around 2500–3000 per nal membrane of the endothelium, which is considered mm ), reduced in phasic skeletal muscle (around 300– to compromise approximately 20% of the intravascular 400 per mm ) and even lower in the bones, fat, connec- volume. It is a multi-component layer composed of pro- tive tissues and in tonic skeletal muscle (less than 100 per teoglycans (including syndecan-1) and glycoproteins, mm ) [31]. anchored to the endothelium by glycosaminoglycans. At the junction between the metarteriole and some Although its role in vascular permeability has recently capillaries, a precapillary sphincter consisting of a single been debated [41], the glycocalyx mediates several key band of smooth muscle may be present that allows regu- physiological processes, such as vascular barrier func- lation of the percentage of capillaries open to erythrocyte tion, hemostasis, autoregulation, leukocyte, and platelet perfusion. However, even if such precapillary sphincters adhesion, and also transmission of shear stress to the have been known for decades, their existence, except underlying endothelium [42]. Jung et al. showed that high within the mesentery [32] and the brain [33], remains syndecan-1 levels, reflecting glycocalyx shedding, were controversial [34]. In some tissues, such as the heart, predictive of short-term mortality in early AMICS [43]. all capillaries are usually open to perfusion, whereas, in Finally, a crucial but under-investigated parameter is some other tissues, such as skeletal muscle and intestine, the interaction between microcirculation and the lym- only 20–30% of capillaries are open. phatic system. Lymphatic vessels are present in almost all In case of need, relaxation of the precapillary sphinc- tissues (except bone marrow, cartilage, and cornea [44]) ter in the latter tissues allows for the recruitment of and their primary function is to drain interstitial fluid more open capillaries and, therefore, an increased tran- and macromolecules to the venous circulation at a total scapillary exchange. Finally, capillaries merge into a ven- volume of almost 8 L/day [45]. In congestive heart fail- ule (~ 10–50 µm), which has a discontinuous, thin layer ure, such as CS, lymphatic contractile dysfunction has of smooth muscle draining into small veins. Changes in been suggested to play an important role to generation venous smooth muscle tone can significantly affect capil - of interstitial edema, causing impairment of blood flow, lary exchange as constriction of the venules leads to an increasing diffusion distance, and cellular hypoxia [46]. increase in capillary pressure, whereas dilation of the However, there are currently no specific drug treatments venules exerts the opposite effect. in clinical use available to reduce lymphatic pump dys- One other important characteristic of microcircu- function [47]. lation is the decrease of hematocrit in the capillaries, known as the Fåhræus effect [35]. Indeed, concentration Microvascular flow regulation of fast-flowing red blood cells in the center of the lumen, Vasoregulation within the microcirculation itself varies and of slower-flowing plasma along the wall of the ves - according to the anatomic topography. Indeed, some of sel, in combination with plasma skimming at bifurcations the vessels of the microcirculation are supported by vas- [36] leads to a reduced red blood cell transit time and a cular smooth muscle (VSM) and others are not. The VSM decreased hematocrit in branching capillary networks. tone is partly modulated by local concentrations of vaso- Recent data found that the Fåhræus effect may increase active metabolites and mediators, autonomic influences in shock states (reducing hematocrit even more) and thus (sympathetic stimulation causes vasoconstriction), and could contribute to further decreased tissue oxygenation hemodynamic factors, but also by conducted responses in low perfusion areas [37]. from downstream vessels [48]. Increases in transmural All the vessels of macro- and microcirculation are pressure also activate mechanosensitive ion channels in almost entirely lined by endothelial cells (EC) which are VSM leading to vasoconstriction, known as the myogenic organ-specific. These EC help maintain organ homeo - response [49]. stasis by regulating various functions including the traf- In addition, the whole microcirculation (even not sur- ficking of fluid, solutes, hormones, and macromolecules rounded by VSM) is also affected by hemodynamic fac - [38]. Frydland et al. reported that AMICS patients had tors in responses to shear stress and circumferential Merdji et al. Annals of Intensive Care (2023) 13:38 Page 6 of 15 wall stress generated by transmural pressure. EC sensed (PPV), the total vessel density (TVD) if all vessels are per- increases in shear stress, which leads to vasodilation due fused, or the perfused vessel density (PVD). The hetero - to the release of mediators including nitric oxide (NO), geneity index reflects heterogeneities in microcirculatory prostaglandins, and EDHF (endothelium-derived hyper- flow caused by endothelial and/or erythrocyte alterations polarizing factor). Under hypoxic conditions, EC can also [53]. Other devices also exist using near-infrared spec- release adenosine, a potent vasodilator [48]. troscopy (NIRS) or assessment of skin blood flow using u Th s, because the capillaries are deprived of muscu - skin laser Doppler imaging [54]. However, these tech- lature and innervation, the flow in each capillary bed is nologies have many limitations [55], among them, lim- mostly driven by the hemodynamic pressures differences ited availability of these different devices, lack of a clearly between the arteriolar pressure/precapillary sphincter defined target value, and limited representativeness of and the postcapillary venules, also named the microcir- microcirculatory impairment in other tissues [55]. culatory driving pressure. This condition is frequently Indirect assessment of the microcirculation can be beneficial, because a single capillary bed can be supplied roughly done by arterial lactate level and its variations; by multiple arterioles, which may allow blood flow to however, due to its well-known limitations [56], it has a increase by 200–500% without any significant change in poor correlation with microcirculatory disorders at the overall arteriolar pressure [50]. For instance, the density organ level [7]. Urine output has also been considered of perfused capillaries may increase from 1000 to 4000/ a traditional marker of tissue perfusion [57] partially mm in the myocardium during maximal workload [51]. reflecting microcirculation; however, it may take time to However, because the main pressure drastically decreases assess, and because diuretics are often used in conges- in the arterioles (resistance vessels), microcirculation at tion and because type 1 acute cardiorenal syndrome are the capillary level is considered a very low-pressure com- frequent in CS, it may be difficult to integrate. Interest - partment. Therefore, mean capillary pressure appears to ingly, surrogate indirect microcirculation assessment can be more influenced by the downstream venous pressure also be done at the bedside using traditional markers of than the upstream arterial pressure. In this perspective, peripheral tissue perfusion signs, such as capillary refill central venous pressure appears to be one of the main time (CRT), mottling, and PCO [58]. These perfusion determinants of capillary blood flow. This is of particular signs are strongly linked with microcirculatory blood concern in CS, where the central venous pressure is often flow alteration in cardiogenic shock [59]. CRT measures very elevated [52]. the time required to recolor the tip of a finger. Mottling Finally, oxygen pressures can be lower in the micro- is defined as patchy skin discoloration that usually starts circulation than that of the venous oxygen levels due to around the knees. Central venous–arterial carbon diox- shunting of the oxygen transport of the microcirculation ide difference ( PCO ), also named Pv-aCO or PCO 2 2 2 from the arterial to the venous compartment which is gap, is the difference between partial pressure of CO in why monitoring the microcirculation directly is impor- venous blood and arterial blood [60, 61]. Although con- tant in identifying its dysfunction [14]. troversial, Ospina-Tascon [60], have well-highlighted the good correlation between the PCO gap and microvas- Assessing the microcirculation cular blood flow during the early phases of septic shock. Nowadays, both direct and indirect methods are available However, this marker has some limitations and may vary to assess microcirculation. Each of these methods pos- depending on specific conditions (HbO saturation [i.e., sesses advantages and disadvantages. the Haldane effect], arterial pH, temperature, and hema - Direct observation of the microcirculation can be done tocrit) [61, 62]. at the bedside, using hand-held vital microscopy, such as Most of these perfusion parameters, such as CRT, have Sidestream Dark-Field (SDF), and Incident Dark-Field been validated with good reproducibility and excellent (IDF) imaging techniques to assess the sublingual micro- interrater concordance [63]. Moreover, they are simple circulation [53]. noninvasive, priceless tools allowing a real-time assess- Analyses of the sublingual microcirculation images ment of microcirculation at bedside; although, in contrast allow assessments of the convective and diffusive com - to analysis of hand-held vital microscopy images, they ponents of the microcirculation [6]. The convective do not give insight into underlying mechanisms asso- component of these functional parameters of the micro- ciated with microcirculatory alterations [53]. Of note, circulation can be described either semi-quantitatively, comparing different peripheral tissue perfusion param - by the microcirculatory flow index (MFI), or quantita - eters in CS, the less relevant seemed to be the central-to- tively, by the use of space–time diagrams. The diffusive peripheral temperature difference, which is the difference component can be described either by a combination of between central temperature and peripheral temperature the De Backer score and proportion of perfused vessels [59], although it was the first variable related to the use M erdji et al. Annals of Intensive Care (2023) 13:38 Page 7 of 15 of the peripheral perfusion as an indicator of circulatory failure and CS [6]. These alterations included a nearly shock, introduced by Weil in the sixties [64]. 50% decreased density of small perfused vessels with numerous non-perfused or intermittently perfused Microcirculation alteration during cardiogenic shock small vessels in CS compared to control patients. A (Fig. 2) marked heterogeneity was also observed between the In 1922, Freedlander et al. were the first to describe different areas. These alterations were also more severe altered microcirculation in patients with cardiac fail- in patients who did not survive. Similarly, Jung et al., ure using nailfold videomicroscopy [65]; however, this reported reduced microvascular perfusion in patients site is particularly sensitive to small changes in exter- with CS, associated with an increased arterial lactate nal temperature. Even though this work was done level [7]. In a prospective cohort study of patients with about 100 years ago, it was not until the beginning of AMICS, low perfused capillary density at admission the twenty-first century that physicians became seri - was strongly and independently associated with 30-day ously interested in microcirculation in CS. Although mortality, with a greater predictive value than the the number of studies about this issue remains very baseline SOFA score [12]. Moreover, an increase in per- limited in indexed databases, such as PubMed to date. fused capillary density after 24 h was significantly asso - In 2000, using venous air plethysmography, Kirschen- ciated with a better outcome. Interestingly, decreased baum et al., measured forearm blood flow in patients capillary blood flow was not correlated with standard with CS before and after arterial occlusion. The authors macrocirculatory parameters, such as heart rate, blood reported an attenuated vascular response to reactive pressure, CI, and cardiac power index (CPI) at admis- hyperemia, which indicates attenuation of the micro- sion. However, it was correlated with pulmonary artery vascular response to hypoxia [66]. Indeed, a normal occlusion pressure (PAOP). physiological response to reactive hyperemia is usu- Recently, a sub-study of the CULPRIT–SHOCK trial ally characterized by an increase in blood flow either assessed the sublingual capillary network using videomi- from capillary recruitment and/or increased velocity croscopy post-percutaneous coronary intervention [68]. of blood flow through previously opened capillaries The study shows that microcirculatory perfusion param - [67]. Using modern sublingual videomicroscopy, De eters have better prognostic value than macrocirculatory Backer et al. showed a high prevalence of microvascu- parameters to predict the combined clinical endpoint of lar blood flow alterations in patients with severe heart 30-day all-cause death and renal replacement therapy Fig. 2 Microcirculation alteration during cardiogenic shock. Alterations of microcirculation can be characterized by multiple different types of impairments, such as no capillary perfusion, low perfusion, heterogeneous perfusion, stasis, or shunting area. Besides, it can also be a result of hemodilution of microcirculatory blood by plasma skimming resulting in the loss of erythrocyte-filled capillaries which decreases tissue oxygen delivery. Or it can be secondary to edema caused by capillary leak syndrome (seen in critically ill patients) which results in increased diffusive distance and reduced ability of the oxygen to reach the tissue cells Merdji et al. Annals of Intensive Care (2023) 13:38 Page 8 of 15 in patients with AMICS. The authors demonstrated tissue pressure and changes the viscosity within the ves- that post-percutaneous coronary intervention (PCI) sel lumen. normotensive CS patients with impaired microvascu- Low systemic vascular resistance or vasopressors, used lar perfusion have a significantly higher risk of mortal - to counteract this vasoplegia [76], may also be respon- ity or renal replacement therapy than normotensive CS sible for the decrease in microvascular perfusion. Vaso- patients with normal microvascular perfusion. This loss pressor may also decrease CO by increasing the afterload of hemodynamic coherence between macrocirculation of an already failing left ventricle. However, De backer and microcirculatory perfusion parameters supports that et al. did not observe any relationship between the doses microvascular perfusion may be a significant determi - of vasoactive agents and microvascular alterations [6], nant for clinical outcome after AMICS, even in normo- whereas Jung et al. found an inverse correlation [77]. tensive CS patients when macrohemodynamic conditions Finally, activation of the coagulation cascade and forma- are restored. tion of microthrombi obstructing the microcirculation These microcirculatory dysfunctions were also seen have been suggested but are unlikely because microvas- using videomicroscopy in patients with CS under veno- cular alterations were also seen in patients treated with arterial extracorporeal membrane oxygenation (VA- multiple anti-aggregation therapies and anticoagulant ECMO) support [69–71]. In a retrospective study based drugs for AMICS [7, 12]. on an indirect perfusion parameter strongly linked with As a concrete illustration, impairment of the micro- microcirculation, a PCO gap > 6 mmHg 6 h after VA- circulation within the lungs may cause the activation of ECMO initiation was associated with early death (under arteriovenous shunts, ultimately leading to the develop- VA-ECMO or less than 72 h after VA-ECMO weaning) ment of atelectasis and hypoxemia [78, 79]. While altered [72]. This increase in the PCO gap cannot be explained microcirculation in the liver may result in functional by inadequate hemodynamic support, as the VA ECMO disturbances, such as impaired synthesis of coagulation flow rates and mean arterial pressure (MAP) were simi - factors [4]. Consequently, acute hepatic dysfunction, lar in both groups, and only a weak correlation was found also known as “shock liver,” results in reduced synthesis between VA-ECMO flow rate and the PCO gap. of protein C and antithrombin, which predisposes the Based on easier-to-assess microcirculation param- individual to microvascular thrombosis [80]. In the gas- eters, the FRENSHOCK prospective study reported that trointestinal tract, microcirculatory disorders during mottling at admission for CS was significantly associ - experimental autoimmune myocarditis have been found ated with 30-day mortality [73]. In another prospective to play a significant role in the deterioration of its entero - observational study of CS patients, a CRT > 3 sec at the cyte barrier function in mice [81]. This intestinal barrier fingertip at admission in ICU was associated with an alteration may potentially allow the translocation of bac- increase 90-mortality or need for VA-ECMO support. teria or endotoxins into the bloodstream, which may con- Furthermore, the combination of CardShock score with tribute to vasoplegia, aggravating the initial CS state [82]. CRT > 3 sec resulted in a greater performance to predict However, using sublingual SDF imaging in an experi- 90-day mortality or VA-ECMO support than CardShock mental preclinical porcine model of CS, Stenberg et al., score alone, improving the AUC to 0.93. CRT was also showed that microcirculation might be initially preserved well-correlated with arterial lactate and mottling but in the first hours of CS despite severe alteration of macro - performed even better than mottling in predicting poor circulation parameters [83] (Fig. 3, adapted from Chion- outcomes. Finally, in the same study, a high PCO gap cel et al., 2020 [84]). Interestingly, in a preclinical murine seemed to be associated with poor outcomes in cardio- model of CS, while sublingual microcirculation was rap- genic shock [59]. idly altered during the initial phase of CS, the cerebral All of these microvascular alterations may be explained cortical microcirculatory flow remained fully preserved, by a decrease microcirculatory driving pressure (defined at least during the first 4 h of CS [85]. These preclinical as the difference between post-arteriolar and venu - results suggest that time (potentially required to induce lar pressure) due to an increase in central venous pres- systemic inflammatory response syndrome) and probably sure during CS, which may act as an outflow obstruction ischemia–reperfusion injury may play a role. of organ perfusion [74]. They may also be explained by an increase in various inflammatory mediators released Can systemic microcirculation be improved in cardiogenic during CS leading to impaired leukocyte [75] and eryth- shock? (see Table 2) rocyte [66] deformability with increased attachment to In the study of De Backer et al., the microvascular blood vessel walls reducing microvascular flow but also lead - flow alterations in patients with severe heart failure and ing to transudation of fluids into the perivascular region CS could be totally reversed with the topical applica- favoring interstitial edema which increases extravascular tion of acetylcholine (using a piece of gauze soaked with M erdji et al. Annals of Intensive Care (2023) 13:38 Page 9 of 15 Fig. 3 Schematic time course of macro- and microcirculatory dysfunction in cardiogenic shock (adapted from Chioncel et al., 2020). While macrocirculatory dysfunction seems to predominate initially during CS, the microcirculation becomes progressively dysfunctional in a second phase. This can ultimately lead to a loss of hemodynamic coherence. MODS multiple organ dysfunction syndrome acetylcholine at a concentration of 10–2 M during 1 min) because capillaries consist of a single layer of epithelium suggesting that the endothelium was still able to respond and a basement membrane not surrounded by smooth to vasodilators and that therapeutic interventions aiming muscle. at opening the microcirculation may be considered [6]. In a prospective comparative study in AHF, Teboul Nitroglycerin, an organic nitrate, such as isosorb- et al. showed that the PCO gap was found to decrease ide dinitrate, acts by providing an exogenous source of while increasing the dose of dobutamine from 0 to 10 μg/ NO which binds to soluble guanylate cyclase, produc- kg/min (p < 0.05) and then to increase slightly, but not ing cyclic guanosine monophosphate (GMP) leading to significantly, when the dose was increased above [90]. vascular smooth muscle relaxation [86]. Den Uil et al. In a sub-study of the IABP–SHOCK II trial which showed that intravenous low-dose nitroglycerin in CS is the first randomized study directly investigating the was associated with an increase in sublingual perfused microcirculation in patients with CS, Jung et al. assessed capillary density but also with a reduction in cardiac fill - perfused capillary densities (< 20 µm), perfused vessel ing pressures (both central venous pressure and PAOP) densities (< 100 µm), total capillary densities and total [87]. In the present case, it is likely that nitroglycerin vessel densities using a SDF intravital microscope [77]. improved microcirculation through both macro and Although the intra-aortic balloon pump (IABP) increases microcirculatory effects. However, because vasodila - MAP and CO (∼0.5 L/min), it does not improve clinical tors induce hypotension, guidelines contraindicate their outcomes in patients with AMICS or their microcircula- use in cases of shock with a systolic BP < 110 mmHg tion. Indeed, results revealed no difference regarding the [23]. Another limitation is nitrate tolerance which may aforementioned microcirculation parameters between develop within 24 h, but this reduced effectiveness may patients treated with or without an IABP. Munsterman be overcome by increasing the dosage. However, no pro- et al. even found that IABP worsens microcirculation in spective study to date has assessed vasodilators, such patients having suffered CS, showing an increase in PVD as nitroglycerin, in association with vasopressors, such of small vessels after withdrawal of IABP [91]. as norepinephrine in CS. This combination which may Recently, in the randomized SHOCK–COOL Trial, seem counterintuitive, using a prostacyclin analog (an mild therapeutic hypothermia (24 h at 33 °C) in patients endothelium-derived relaxing factor), is currently being after primary percutaneous coronary intervention for evaluated in septic shock [88]. It is noteworthy that most AMICS did not show any substantial benefit on macro data show no deleterious effect of norepinephrine on (CPI in the first instance) and microcirculation (assess microcirculation [89], which could be explained partly using sublingual videomicroscopy) and also no clinical Merdji et al. Annals of Intensive Care (2023) 13:38 Page 10 of 15 ff ff ff ff Table 2 Impact on macro- and microcirculation of drug and mechanical circulatory support devices used in cardiogenic shock Drugs/MCS devices Mechanism of action Study protocol Eects on macrocirculation Eects on microcirculation Study [Ref ] described in the study described in the study Dobutamine β adrenergic receptor agonist Dobutamine was given when Increase HR, CI and SvO No effect on microcirculation Den Uil et al., PMID: 25084171 1 2 CI was < 2.2 L/min/m or SvO Slight reduction of PAOP was < 65% Levosimendan Myofilament calcium sensitizer No study in cardiogenic shock (An abstract, published in German in 2009 in Clin Res Cardiol seems to show improvement of microcirculation) Milrinone Phosphodiesterase-3 inhibitors No study in cardiogenic shock increasing intracellular calcium by inhibiting the degradation of cAMP Enoximone Phosphodiesterase-3 inhibitors Enoximone was given when Decrease CVP and PAOP Increase PCD Den Uil et al., PMID: 25084171 increasing intracellular calcium CI was < 2.2 L/min/m or SvO by inhibiting the degradation of was < 65% cAMP Norepinephrine α and β adrenergic receptor Norepinephrine was given to Increase MAP Slight non-significant reduction Den Uil et al., PMID: 25084171 1 1 agonist patients when MAP of PCD was < 60 mmHg, independent of CI or SvO , to reach a target MAP ≥ 70 mmHg Norepinephrine was given to Increase MAP Increase delta StO and StO Perez et al., PMID: 24509521 2 2 increase MAP from 65–70 to recovery slope (NIRS) 80–85 mmHg Epinephrine Stimulates both α and β No study in cardiogenic shock 1 1 adrenergic receptors Nitroglycerin Organic nitrate providing an Infusion was started at 8 µg/min Increase CI Increase in PCD Den Uil et al., PMID: 19639300 exogenous source of NO and then doubled every 30 min Decrease MAP, CVP and PAOP up to 133 µg/min IABP Intra-aortic balloon inflating IABP was inserted in AMICS Eect on microcirculation not No effect on microcirculation Jung et al., PMID: 25720332 during diastole to increase described in this study coronary perfusion and deflat - IABP was withdrawn in Withdrawal of IABP led to a Withdrawal of IABP led to an Munsterman et al., PMID: ing during systole to decrease recovering CS patients decrease in MAP and an increase increased PVD 20738876 afterload in diastolic arterial pressure Intentional Eect on microcirculation not IABP stop led to a decrease MFI Jung et al., PMID: 19367424 stop of IABP support in CS described in this study M erdji et al. Annals of Intensive Care (2023) 13:38 Page 11 of 15 ff ff Table 2 (continued) Drugs/MCS devices Mechanism of action Study protocol Eects on macrocirculation Eects on microcirculation Study [Ref ] described in the study described in the study VA-ECMO Percutaneous cardiopulmonary VA-ECMO implantation in Reduce HR and LVEF Increase PPV, MFI and perfused Chommeloux et al., PMID: bypass providing full hemody- refractory CS SVD 31634235 namic support and increasing Under VA-ECMO: increasing While increasing dobutamine: No effect on microcirculation Chommeloux et al., PMID: afterload dobutamine above 5 μg/kg/min increase HR and AoVTI while increasing dobutamine or 35700546 or VA-ECMO flow While increasing VA-ECMO-flow: VA-ECMO-flow increase HR Under VA-ECMO inserted within No change in MAP while Both contradictory and non- Wei et al., PMID: 33898485 48 h: increasing VA-ECMO pump increasing VA-ECMO pump flow contradictory flow or decreasing VA-ECMO responses of sublingual pump flow microcirculation Probability of increasing PVD after increasing VA-ECMO pump flow were higher in the events with a PVD < 15 mm/mm at baseline Under VA-ECMO in patient with Increase HR and MAP No differences were observed in Du et al., PMID: 27983541 MAP < 60 mmHg: inotropic and Thenarmuscle StO and cerebral vasopressor agents (dopamine, rSO dobutamine, norepinephrine or Thenar muscle StO desaturation epinephrine) were administered slope and resaturation slopes to target and maintain a MAP at during the vessel obstruction 60–90 mmHg test were also unchanged Impella Temporary percutaneous Impella LP2.5 was inserted after Increase LVEF Increase PVD and MFI Lam et al., PMID: 19280085 LVAD with a nonpulsatile axial PCI for a first anterior STEMI (No flow pump that propels blood CS in this study but acute heart from the left ventricle into the failure) ascending aorta through the catheter AMI acute myocardial infarction, AMICS acute myocardial infarction complicated by cardiogenic shock, AoVTI aortic velocity–time integral, CI cardiac index, CS cardiogenic shock, CVP central venous pressure, IABP intra-aortic balloon pump, LVAD left ventricular assist device, LVEF left ventricular ejection fraction, MCS mechanical circulatory support, MFI microvascular flow index, PAOP pulmonary artery occlusion pressure, PCD perfused capillary density, PCI percutaneous coronary intervention, PPV proportion of perfused vessel, PVD perfused vessel density, SVD small-vessel density, STEMI ST-element elevation myocardial infarction, VA-ECMO veno-arterial extracorporeal membrane oxygenation Merdji et al. Annals of Intensive Care (2023) 13:38 Page 12 of 15 benefit in survival [92]. Suggesting no benefit of mild Conclusion hypothermia in CS. Cardiogenic shock is characterized by microcirculatory To date, there is very limited data showing a drug bene- dysfunction. Restoration of macrocirculation parameters fit, whether inotropic or vasopressor agents, on microcir - is the primary goal in the management of CS. However, culation in CS [89]. In a small study, Enoximone tested in one goal of therapy for CS should also be the restoration ten CS shows a microcirculation improvement in CS [93]. of microcirculatory blood flow and thus recover oxygen Moreover, increasing MAP from 65–70 to 80–85 mmHg supply to sustain cellular function. Recent devices such with norepinephrine in AMICS was associated with an as hand-held vital microscopy, and also “easy to use, easy improved microcirculation as assessed by thenar NIRS to learn” priceless perfusion parameters (such as capillary measurements [94]. However, most of these patients refill time and mottling) have been established as reli - were post-cardiac arrest CS generally presenting with a able tools for assessing microcirculation alteration during shock state different from standard CS [95, 96]. CS. Although the relationship between the persistence In a study assessing microcirculation in refractory CS of microcirculation abnormalities and prognosis seems patients supported by VA-ECMO, almost all microcircu- established in CS, further studies are needed to better lation parameters, except small vessel density, improved define in which patients, in which timing, under which 12 h after VA-ECMO initiation [97]. Interestingly, in this monitoring, patient’s microcirculation disturbances study, the inability to rapidly normalize microcirculation should specifically be treated in cardiogenic shock. parameters during the first 24 h of VA-ECMO support, despite normal macrocirculation parameters, was asso- Abbreviations ciated with mortality. Moreover, microcirculatory flow AHF Acute heart failure response as a result of 50% pump flow decrease from AMI Acute myocardial infarction AMICS Acute myocardial infarction complicated by cardiogenic shock the baseline visualized by hand-held vital microscopy BP Blood pressure occurring during VA-ECMO reliably predicted success CI Cardiac index of weaning [69]. These results were confirmed in a study CO Cardiac output CRT Capillary refill time by Wei et al., however, in addition they also identified CS Cardiogenic shock that some patients paradoxically showed a reduction in GMP Guanosine monophosphate microcirculatory flow after an increase in VA-ECMO IABP Intra-aortic balloon pump ICU Intensive care unit pump flow [70]. Similarly, successful improvement of LVEF Left ventricular ejection fraction perfused small vessel density within the first 24 h of VA- MFI Microcirculatory flow index ECMO initiation was able to accurately predict in-ICU NIRS Near-infrared spectroscopy PPV Proportion of perfused vessel mortality [71]. PVD Perfused vessel density Using NIRS, microcirculatory assessment showed SCAI Society for Cardiovascular Angiography and Interventions no benefit when increasing MAP from < 60 mmHg to SBP Systolic blood pressure TVD Total vessel density 60–90 mmHg in CS patients on VA-ECMO support [98]. VA-ECMO V enoarterial extracorporeal membrane oxygenation Likewise, combined IABP and VA-ECMO support did not show any benefit on microcirculation parameters Acknowledgements None. [99]. A French study found that when macrocirculation has already been restored in patients with VA-ECMO- Author contributions supported refractory CS, increasing dobutamine HM and FM wrote the first draft of the manuscript. BL, CJ, CI, and MS partici- pated in the revision of the manuscript. All authors approved the final manu- (above 5 μg/kg/min) or ECMO flow did not further script. H.M. created the figure with BioRenders.com (https:// biore nder. com/) improve microcirculation [100] even if it did improve subscribed to H.M. All authors read and approved the final manuscript. macrocirculation. Funding Finally, in a very small study, assessing sublingual No funding to declare. microcirculation in six patients with pre-shock due to ST-element elevation myocardial infarction (STEMI) Availability of data and materials Not applicable. treated with primary PCI, Impella LP2.5 significantly improved microcirculation parameters compared with Declarations the non-support group [101]. Remarkably, restoration of the systemic microcirculation occurred within 24 h of Ethics approval and consent to participate Impella support. Not applicable. Consent for publication All authors hereby consent to the publication. M erdji et al. Annals of Intensive Care (2023) 13:38 Page 13 of 15 Competing interests 14. Ince C, Sinaasappel M. Microcirculatory oxygenation and shunting in Prof. Can INCE who is chief scientific officer of Medical BV, Leiden, The Neth- sepsis and shock. Crit Care Med. 1999;27(7):1369–77. erlands, a company that provides devices, software, education, and services 15. 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Annals of Intensive Care – Springer Journals
Published: May 6, 2023
Keywords: Cardiogenic shock; Heart failure; Microcirculation; Macrocirculation; Perfusion parameters
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