Aneurysmal subarachnoid hemorrhage (aSAH) is a worldwide health burden with high mortality and permanent disability rates.1,2 Brain damage does not only occur at the moment of the initial hemorrhage but evolves over hours and days.3 Moreover, the detrimental effects of aSAH are not limited to the cerebral event; up to 80% of patients4 develop medical complications including cardiac, pulmonary, renal, hepatic, hematological, metabolic, and endocrine dysfunction.5–10 In particular, myocardial dysfunction and pulmonary edema,11–13 which can lead to hypotension and hypoxia and worsened secondary brain injury, as well as impacting the onset of delayed cerebral ischemia (DCI) and vasospasm,5 are common.
Standard hemodynamic monitoring in the intensive care unit (ICU) includes fluid balance assessment, invasive arterial pressure, and central venous pressure measurements.14–16 Because of the complexity of the clinical manifestations of aSAH, and the involvement of the brain-heart-lung axis, the use of advanced hemodynamic monitoring modalities, such as pulse index continuous cardiac output (PiCCO), pulse dye densitometry, and pulmonary artery catheterization, has been proposed by several authors.14,16–23 However, advanced monitoring techniques can be precluded in some cases because of the complexity and risks related to thermodilution techniques, particularly those involving pulmonary artery catheterization.24–28
The optimal strategy for the assessment and management of cardiac dysfunction after aSAH remains unclear.23 In particular, no definitive evidence is available on the need for hemodynamic monitoring in this patient cohort, and questions remain whether standard compared with advanced hemodynamic monitoring techniques can effectively improve patient care and clinical outcomes.
We, therefore, conducted a systematic review and meta-analysis to investigate the available literature with regard to hemodynamic monitoring after aSAH. The aim was to assess whether a clinical strategy guided by standard compared with advanced hemodynamic monitoring can reduce systemic and cerebral complications, as well as improving patient outcomes.
This systematic review and meta-analysis adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis—Protocols (PRISMA-P) guidelines29 and followed the PRISMA checklist (PRISMA-DTA checklist and abstract checklist for PRISMA-DTA). The protocol was registered with the International Prospective Register of Systematic Reviews (PROSPERO) on December 18, 2018 (registration number: CRD42018116427).
Data Sources, Search Strategy, and Screening Selection
A systematic literature search was performed for articles published between January 1, 2000 and January 1, 2019 using the following electronic databases: PubMed, Scopus, SciVerse ScienceDirect, Web of Science PubMed, EMBASE, and the Cochrane Central Register. The search was performed using the following terms: “volume,” “hemodynamic,” “management,” “monitoring,” “aneurysmal,” “subarachnoid hemorrhage.” Reference lists of the prescreened studies were manually checked, using an iterative approach.
For the systematic review, we included studies involving aSAH patients admitted to the ICU and subjected to any type of hemodynamic monitoring. From this pool of studies, we selected those eligible for quantitative synthesis and meta-analysis, including only randomized controlled trials describing aSAH patients admitted to the ICU undergoing standard versus advanced hemodynamic monitoring and reporting as outcomes the occurrence of cardiorespiratory complications (pulmonary edema), and/or neurological complications (DCI), and/or neurological outcome (modified Rankin Scale), and/or fluid balance/intake. We merged all monitoring tools into 2 predefined groups. In the standard monitoring group, we included all hemodynamic monitoring methods commonly used in all aSAH patients admitted to the ICU: arterial pressure, central venous pressure, and evaluation of fluid balance. In the advanced monitoring group, we included hemodynamic monitoring techniques that provide more structured information than standard methods, including cardiac output, stroke volume variation, or circulating blood volume, and more complete measurements obtained through thermodilution techniques (extra lung water index, global end-diastolic volume index, etc.).
Only original studies published in English in peer-reviewed journals were considered for inclusion in this review. Studies conducted in healthy volunteers or in animal models were excluded. Editorials, commentaries, letters to the editor, opinion articles, reviews, meeting abstracts, were also excluded, as well as original articles lacking an abstract and/or quantitative information. When multiple publications from the same research group/center described case series that were potentially overlapping, we used the most recent publication, if eligible. More details about data extraction are reported in the Supplementary Material (Supplementary Digital Content 1, http://links.lww.com/JNA/A252: Table showing the extracted data in each study assessed for eligibility).
Exclusion criteria used to further evaluate the pool of studies preliminarily selected for the qualitative synthesis were as follows: (1) case reports and studies including a small number of patients (<10); (2) studies conducted in the operating room or in the perioperative period only; (3) subarachnoid hemorrhage not of aneurysmal cause; (4) triple-H therapy or use of vasoactive medications as the endpoint of the study; (6) studies discussing only cerebral hemodynamic monitoring; (7) studies for which only an abstract was available; (8) studies including patients with other types of brain injury wherein data on those with aSAH could not be separately identified.
All studies were independently screened by 2 authors (C.R., F.S.) looking at study titles and abstracts for potential eligibility. Screening questions were answered and pilot tested with a subset of records before implementation. Disagreement was assessed using κ statistics and resolved through discussion; a third reviewer (L.B.) was involved if necessary.
Appraisal of Study Quality
Two reviewers were content experts (C.R., F.S.) and 1 reviewer (L.B.) an experienced biostatistician. The content experts assessed potential publications with respect to the appropriateness of the research questions tested, whereas the biostatistician evaluated the appropriateness of the methods used. Disagreement was resolved by consensus.
Strength Assessment of the Scientific Evidence
The strength of the body of evidence was assessed according to the Grading of Recommendations, Assessment, Development and Evaluations (GRADE)30 evidence system (Supplemental Digital Content 2, http://links.lww.com/JNA/A253: Table showing the quality of evidence for each study included in the meta-analysis). We used the modified Cochrane Collaboration tool to assess the risk of bias for the 3 randomized controlled trials selected for meta-analysis.31
A meta-analysis was performed to evaluate the onset of DCI as the primary outcome, and pulmonary edema onset, fluid intake, and poor neurological outcome (modified Rankin Scale scores 4 to 6) as secondary outcomes.
For dichotomous outcomes, we calculated the relative risk (RR) and 95% confidence intervals (CIs). For continuous outcomes, we computed the mean difference. All estimates were calculated with a mixed-effects model and the Der Simonian-Laird method. Statistical heterogeneity was assessed with the Cochran Q statistic and quantified with the I2 statistic. Clinical heterogeneity was also assessed. Publication bias was assessed by visual inspection of funnel plots; formal testing of asymmetry was avoided, as, for all outcomes, the number of included studies was below 10.32 All analyses were performed with R 3.2.3 and the metafor package (The R Foundation for Statistical Computing, www.r-project.org). Statistical significance was considered for 2-tailed P-value <0.05.
Characteristics of the Studies Included in the Systematic Review
The initial database search returned 708 records. After removing duplicates and screening records, 58 full-text articles were assessed for eligibility, and 44 of these did not meet the eligibility criteria. We finally selected 14 studies for the qualitative synthesis and 3 studies for quantitative analysis (Fig. 1). Agreement of selected studies by the 2 reviewers was achieved in 100% of cases. The studies included in the qualitative analysis included randomized trials; prospective, observational, and comparative studies; multicenter prospective cohort studies; and retrospective observational design studies including consecutive adult aSAH patients. The main characteristics, study typology, aims, main findings, and results of all the selected studies are shown in the Supplementary Material: 7 studies14–17,21,33,34 evaluated 2 types of hemodynamic monitoring (Supplemental Digital Content 3, http://links.lww.com/JNA/A254: Table summarizing the main characteristics of the studies comparing 2 types of hemodynamic monitoring; Supplemental Digital Content 4, http://links.lww.com/JNA/A255: Table summarizing main findings and results of studies comparing 2 types of hemodynamic monitoring), and 7 studies13,18–20,22,25,35 evaluated a single type of hemodynamic monitoring (Supplemental Digital Content 5, http://links.lww.com/JNA/A256: Table summarizing the main characteristics of studies discussing one type of hemodynamic monitoring, and Supplemental Digital Content 6, http://links.lww.com/JNA/A257: Table summarizing the main findings and results of studies discussing one type of hemodynamic monitoring). PiCCO monitoring was investigated in 10 studies13,15–19,21,22,25,34 and pulse dye densitometry in 4 studies.14,20,33,35
Three studies14–16 comparing 2 different hemodynamic monitoring techniques and including neurological status and/or cardiopulmonary complications and/or fluid intake/balance as outcomes were included in the meta-analysis. We extracted data from these 3 studies, including the prevalence of dichotomous outcomes (DCI, pulmonary edema, neurological outcome) and continuous outcomes (fluid intake and fluid balance) for both control and intervention groups (Supplemental Digital Content 7, http://links.lww.com/JNA/A258: Table showing the derived data from the 3 studies in the meta-analysis). Two studies compared standard hemodynamic monitoring with PiCCO,15,16 and one study compared standard hemodynamic monitoring with pulse dye densitometry.14 The development of DCI, neurological outcome (modified Rankin Scale), and pulmonary edema onset were reported in all 3 studies,14–16 and fluid intake in 2 studies.14,16 We evaluated the risk of bias for the 3 studies selected for meta-analysis (Supplemental Digital Content 8, http://links.lww.com/JNA/A259: Fig. showing risk of bias in the 3 studies included in the meta-analysis).
In the meta-analysis, the pooled incidence of DCI was greater in patients undergoing standard compared with advanced hemodynamic monitoring (RR=0.71, 95% CI=0.52-0.99, P=0.044; heterogeneity I2=0%, 95% CI=0%-73%, P=0.68; number needed to treat 11, 95% CI=7-313) (Fig. 2A). There was no statistically significant difference between the groups managed with standard compared with advanced hemodynamic monitoring in terms of poor neurological outcome (RR=0.83, 95% CI=0.64-1.06, P=0.14; heterogeneity I2=0%, 95% CI=0%-78%, P=0.62) (Fig. 2B), pulmonary edema onset (RR=0.44, 95% CI=0.05-3.92, P=0.46; heterogeneity I2=74%, 95% CI=15%-92%, P=0.02) (Fig. 3A), and fluid intake (mean difference=−169 mL, 95% CI=−1463 to 1126 mL, P=0,8; heterogeneity I2=96%, 95% CI=90%-99%, P<0.01) (Fig. 3B). Funnel plots for the primary outcome (DCI) are shown in Figure 4, and funnel plots for secondary outcomes (pulmonary edema onset, poor neurological outcome, and fluid intake) in the Supplementary Material (Supplemental Digital Content 9, http://links.lww.com/JNA/A260: Fig. of funnel plots for pulmonary edema onset, poor neurological outcome, and fluid intake).
The results of our systematic review and meta-analysis suggest that patients with aSAH may benefit from advanced hemodynamic monitoring. Advanced hemodynamic monitoring–guided management may lead to a reduction in the incidence of DCI, but has no impact on pulmonary edema onset, fluid management, and neurological outcomes. However, the high degree of clinical and possibly statistical heterogeneity in the studies included in the meta-analysis mean that these results can only be considered as hypothesis-generating.
aSAH produces a primary brain injury from intracranial consequences such as hematoma, intracranial volume redistribution, and a dramatic increase in intracranial pressure with a consequent reduction in cerebral perfusion pressure. As a result of the aSAH-induced systemic release of catecholamines,36 patients can also develop secondary cardiopulmonary dysfunction leading to hypoxia, hypotension, and cerebral hypoperfusion.19,25 DCI is one of the main causes of severe disability and death after aSAH, and its occurrence is associated with hemodynamic dysfunction and instability.37,38 Patients with aSAH, especially those with cerebral vasospasm and/or DCI, require meticulous maintenance of intravascular volume status and iatrogenic induction of hypertension through fluid administration and vasopressors, respectively.39,40 The treatment of cerebral vasospasm and DCI can itself lead to cardiovascular dysfunction and pulmonary edema.39,41–46 Optimal hemodynamic management, both in the early and late phases after aSAH, can be challenging because of the complex interactions between the brain, lungs, and heart.
The literature on this topic is lacking, and the key question, can hemodynamic monitoring lead to a reduction in the number of systemic and cerebral complications and thereby improve aSAH outcomes, remains unanswered. Recommendations from the Neurocritical Care Society’s multidisciplinary consensus conference with regard to hemodynamic monitoring in aSAH patients24 are not conclusive and suggest the following (and they are): (1) targeting normovolemia, especially in cases of pulmonary edema or acute lung injury, with standard management of heart failure (high or moderate-quality evidence); (2) that cardiac output monitoring could be a useful tool in patients with evidence of hemodynamic instability or myocardial dysfunction (low or poor quality evidence); (3) avoiding central venous pressure as a target for fluid management; and (4) the routine use of pulmonary artery catheters is not recommended.23
Different hemodynamic monitoring techniques have been proposed in critically ill patients,47 including PiCCO, pulmonary artery catheters, pulse dye densitometry, and FloTrac Vigileo (Table 1). The results of our review show that only a limited number of studies have explored the risks and benefits of using standard versus advanced hemodynamic monitoring techniques in aSAH patients. In one study, hypovolemia, reduction of cardiac index, increase in systemic vascular resistance index, and significantly lower global end-diastolic volume index were associated with DCI onset.19 In a multicenter prospective cohort study, significant differences in global end-diastolic volume index were detected between DCI and non-DCI groups (783±25 vs. 870±14 mL/m2, respectively; P=0.007), with a global end-diastolic volume index threshold of 822 mL/m2 being correlated with the development of DCI.13 In a prospective observational study, Kasuya et al35 analyzed changes in circulating blood volume in aSAH patients using indocyanine green pulse spectrophotometer and found a four fifth reduction in blood volume in the postoperative period with respect to preoperative values; there was a gradual return to normal after ∼7 days. Mutoh et al15 showed that, among aSAH patients with poor admission neurological status (World Federation of Neurological Societies IV to V), those treated with early goal-directed therapy received a lower volume of fluid and had a lower incidence of iatrogenic pulmonary edema compared with patients treated with standard therapy. Moreover, early goal-directed therapy was linked to a lower incidence of DCI (P=0.036), a better outcome at 3 months (P=0.026), and shorter duration of ICU stay (P=0.043) compared with standard care. Similarly, other authors have suggested that transpulmonary thermodilution monitoring–guided treatment is associated with a lower incidence of DCI (P=0.03) and vasospasm (P=0.03) compared with management guided by standard monitoring techniques.16
TABLE 1 -
Available Techniques of Hemodynamic Monitoring
||CO and afterload data
||Partial CO2 rebreathing (Fick’s principle)
||Only in sedated patients under volume control ventilation Less reliable in case of pulmonary disease
|PDD, ICG pulse spectrophotometry
||Indicator dilution technique using indocyanine green (no radioactive tracer) combined with the principle of pulse spectrophotometry (uncalibrated system)
||Circulating blood volume
||The pulse-spectrophotometric signal can be distorted by movement or by inadequate tissue perfusion
|Vigileo (Flotrac) MostCare (PRAM) ClearSight CNAP pulseCO (LiDCOrapid)
||Arterial pressure waveform derived
||Minimally invasive (peripheral arterial catheterization)
||Need for optimal arterial signal PPV less reliable: low HR/RR ratio, irregular heartbeats, mechanical ventilation with low tidal volume, increased abdominal pressure, thorax open, spontaneous breathing
|PiCCO, LiDCO, EV-1000
||Calibrated (intermittent, continuous)
||Invasive (peripheral arterial catheterization+central venous catheterization)
||Invasiveness Need for dedicated catheter
|Pulmonary artery catheter
||Calibrated (intermittent, semicontinuous, fast-respiratory)
||Very invasive (catheterization of pulmonary artery)
||Training required Invasiveness and numerous complications: pulmonary artery perforation, pulmonary infarction, cardiac arrhythmias, sepsis and infections, complete block and/or cardiocirculatory arrest, anatomic damage (eg, at the valve level), pneumothorax, thrombosis
|BioZ, ECOM, Lifegard NICOM
||Changes of systemic vascular resistance and of intrathoracic fluid can affect the measurements Not applicable in thoracic surgery
||Pulse contour system
||Its accuracy still needs improvements and decreases in case of high peripheral resistance, hypothermia, low CO and fingers’ edema
Overview of different types of hemodynamic monitoring currently in use.
CBV indicates circulating blood volume; CFI, cardiac function index; CO, cardiac output; CVP, central venous pressure; dP/dt, left ventricle contractility index; ELW, extra lung water; GEDV, global end-diastolic volume; HR, heart rate; IAP, invasive arterial pressure; ITBV, intrathoracic blood volume; PAP, pulmonary arterial pressure; PCWP, pulmonary capillary wedge pressure; PDD, pulse dye densitometry; PPV, pulse pressure variation; RR, respiratory rate; RVEDV, right ventricular end-diastolic volume; RVEF, right ventricular ejection fraction; SV, stroke volume; SVR, systemic vascular resistance; SVV, stroke volume variation.
Pulmonary edema is a critical complication after aSAH.33 It typically has a biphasic onset with different mechanisms causing early and delayed phase pulmonary edema. In this context, it has been suggested that the global end-diastolic volume index (which measures cardiac preload), extra lung water index, cardiac index, and pulmonary vascular permeability index could be important variables to guide optimal goal-directed therapy.22 However, the results from the present systematic review suggest that advanced hemodynamic monitoring techniques have no impact on the development of pulmonary edema or neurological outcomes. This finding might be explained by the fact that neurological outcomes are influenced not only by the development of DCI, but also by the occurrence and management of other cerebral and systemic complications, including hypoxia, hypovolemia, and hypotension. Furthermore, it can be hypothesized that pulmonary edema onset may be affected by the timing of the application of advanced hemodynamic monitoring. Our results also show great heterogeneity in pulmonary edema onset and fluid intake outcomes. The explanation for this can likely be found in the similar heterogeneity of aSAH patients’ management, which is not based on specific guidelines but mainly led by individual centers’ best practice. We, therefore, propose a decision flowchart to guide the use of advanced hemodynamic monitoring tools in aSAH patients on the ICU (Fig. 5). Reflecting on our own clinical practice, and the results from this systematic review and the meta-analysis, we suggest using advanced hemodynamic monitoring in the following cohorts of aSAH patients: those with poor grade aSAH, those developing neurological complications such as DCI and vasospasm (diagnosed clinically and/or by neuroimaging), those with cardiovascular and pulmonary complications (such as pulmonary edema, neurogenic stunned myocardium), those requiring high doses of vasoactive drugs to maintain adequate cerebral perfusion pressure, and those in whom intravascular volume and hemodynamic status are difficult to interpret.
Our systematic review and meta-analysis has several limitations. The assessment of the quality of studies found that those selected for the meta-analysis have their own, inherent, limitations. Our review focused on specific questions, predefined by a particular category of patients, comparisons, and multiple outcomes. While the search for relevant studies was exhaustive,48 and the assessment of studies was reproducible, the meta-analysis included only a few trials with small numbers of events that have wide CIs. Furthermore, the intervention groups included heterogeneous monitoring techniques, with the possibility of introducing bias. Thus, the credibility of this systematic review and meta-analysis is low-to-moderate, and the confidence in the effect estimates is considered low due to the inherent limitations, imprecision, and risk of bias in all the studies included in the meta-analysis. Even for the outcomes for which the I2 statistics estimate was low, the limited number of studies in the meta-analysis results in an extremely wide CI of this estimate. This means that, at an alpha level of 0.05, we cannot rule out that the actual statistical heterogeneity is high. Therefore, despite some studies showing a benefit from the use of advanced hemodynamic monitoring in aSAH patients,13,17,19–21,25 their limitations preclude a clear evidence-based recommendation for the application of these monitoring techniques in clinical practice.
We identified very low-quality evidence to support the use of advanced hemodynamic monitoring in aSAH patients. Because of the small number and poor quality of the studies included in this systematic review and meta-analysis, the decision to use hemodynamic monitoring in aSAH patients, and the type of monitoring, should be made on a case-by-case basis considering patient characteristics, risks and benefits of monitoring, and individuals’ neurological status and likely prognosis. Further studies are warranted to investigate the hypothesis that clinical management guided by standard compared with advanced hemodynamic management might reduce systemic and cerebral complications after aSAH, as well as improving patient outcomes.
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