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Use of the Fluid Challenge in Critically Ill Adult Patients: A Systematic Review

Messina, Antonio MD, PhD*; Longhini, Federico MD; Coppo, Corinne MD; Pagni, Aline MD; Lungu, Ramona MD; Ronco, Chiara MD; Cattaneo, Marco Ambrogio MD; Dore, Simone PhD§; Sotgiu, Giovanni MD§; Navalesi, Paolo MD, FERS

doi: 10.1213/ANE.0000000000002103
Critical Care and Resuscitation
Free
SDC

The fluid challenge (FC) aims at identifying patients in whom fluid administration improves hemodynamics. Although the FC has been extensively studied, the implementation and definition of improvement are not standardized. This systematic review of studies published between January 1, 1994 and December 31, 2014 characterizes these key components of the FC for critically ill adult patients, as described in the medical literature in the last 20 years. A literature search was performed using MEDLINE, Embase, and Cochrane. For each study, data were collected on study design, study size, study setting, patient population, and how the FC was administered. Eligibility criteria for FC were (1) the infusion of a definite quantity of fluid, (2) of a specific type, (3) in a fixed time period (expressed as either span or infusion rate), (4) with a defined hemodynamic variable as the target, and (5) for a predetermined threshold. One hundred fifty-seven full-text manuscripts were extracted from 870 potentially relevant studies. The inclusion criteria were met by 71 studies including 3617 patients. Sixty-six studies were from a single center and 45 were prospective observational in format. The most common amount infused was 500 cc, used by 55 (77.5%) studies. The most commonly infused fluids were colloids (62.0%). In 43 (60.5%) studies, the FC was administered between 20 and 30 minutes. A positive response to fluid administration was defined as an increase ≥15% of cardiac index or cardiac output in 44 (62.6%) studies. Static or dynamic physiologic indices were utilized in a minority of studies (16.9%) and safety limits for interrupting the FC are adopted in 4 (5.6%) studies only. This systematic review indicates that the FC most commonly consists in infusing 500 mL of crystalloids or colloids in 20–30 minutes, and considered an increase in cardiac index ≥15% as a positive response. However, definite standards for FC administration and evaluation remain undefined.

Published ahead of print May 12, 2017.

From the *Anesthesia and Intensive Care Medicine, Maggiore della Carità University Hospital, Novara, Italy; Anesthesia and Intensive Care Medicine, Sant’Andrea Hospital (ASL VC), Vercelli, Italy; Department of Translational Medicine, Università del Piemonte Orientale “Amedeo Avogadro,” Alessandria-Novara-Vercelli, Italy; §Clinical Epidemiology and Medical Statistics Unit, Department of Biomedical Sciences, University of Sassari, Research, Medical Education and Professional Development Unit, AOU Sassari, Sassari, Italy; and Anesthesia and Intensive Care, Department of Medical and Surgical Sciences, Magna Graecia University, Catanzaro, Italy.

Accepted for publication February 28, 2017.

Published ahead of print May 12, 2017.

Funding: None.

The authors declare no conflicts of interest.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s website.

Potential conflicts of interest unrelated to the present study: Dr Navalesi’s research laboratory has received equipment and grants from Maquet Critical Care, Draeger, and Intersurgical S.P.A. He also received honoraria/speaking fees from Maquet Critical Care, Draeger, Breas, Philips, Resmed and Hillrom. Dr Navalesi contributed to the development of the helmet Next, whose license for patent belongs to Intersurgical S.P.A., and receives royalties for that invention.

Reprints will not be available from the authors.

Address correspondence to Paolo Navalesi, MD, FERS, Anesthesia and Intensive Care, Department of Medical and Surgical Sciences, Magna Graecia University, Viale Europa – Loc. Germaneto, 88100, Catanzaro, Italia. Address e-mail: pnavalesi@unicz.it.

Critically ill patients often receive fluids to increase blood pressure or cardiac output (CO) by increasing the cardiac stroke volume (SV).1,2 The fluid challenge (FC) is a diagnostic approach to hemodynamic management which aims at identifying the patients who respond to fluid administration with an increase in blood pressure or CO.3 In this way, the FC can identify patients for whom use of inotropes or vasopressors is the appropriate strategy. Therapeutically, a positive FC suggests that fluid administration should be continued as long as the response to FC is positive.4 The decision to stop fluid administration occurs when a negative response to FC occurs.

A patient is considered responsive to FC when hemodynamic improvement is observed after volemic expansion. While consensus exists on the use of FC to assess preload responsiveness,1,5 the type of fluid, extent and rate of administration, and hemodynamic targets (either variable and thresholds) are not standardized in clinical practice. Cecconi et al, 1 after reviewing the key components of the FC and its clinical use in the intensive care unit (ICU), proposed the infusion of a standard volume of 200 mL (or 3 mL/kg) in 5 minutes, while guidelines for ICU management of patients with severe sepsis and septic shock propose 500–1000 mL of crystalloids or 300–500 mL of colloids in 30 minutes.6 By affecting the extent of fluid responsiveness and hence the rate of responders, varying criteria for performing the FC and assessing the result FC may limit comparability among studies.

Two large observational studies indicate that both the mode of administration and assessment of the FC in the current clinical practice vary considerably between countries and over time.7,8 In particular, the 2015 FENICE trial, a recent prospective observational study performed in 311 ICUs located in 46 countries, found significant variability with respect to the amount and type of fluid and the rate of administration.8 To address this issue, we systematically reviewed existing literature to evaluate whether the FC in critically ill patients is consistent among studies along the last 2 decades with respect to (a) amount and kind of fluid administration, (b) time of infusion, (c) hemodynamic variables and thresholds for fluid responsiveness, and (d) safety limits.

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METHODS

Study Selection and Inclusion Criteria

For the purposes of this review, we defined FC as the infusion of a definite quantity of fluid of a specific quality in a fixed time (expressed as either span or infusion rate), and defined the outcome of the FC as a change in a defined hemodynamic variable for a predetermined threshold.

We included the following hemodynamic variables as potential indicators of a positive FC: CO, cardiac index (CI), SV, SV index (SVI), or surrogate SV estimations, ie, aortic velocity-time integrals and aortic blood flow, as assessed by either transthoracic or transoesophageal echocardiography. Only articles published in indexed scientific journals between January 1, 1994 and December 31, 2014 in the English language were considered. We selected studies enrolling more than 20 ICU patients receiving at least one FC. Reviews, case reports, and studies published in abstract form were not considered.

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Search Strategy

Two authors (A.M. and F.L.) independently searched MEDLINE, EMBASE, and the Cochrane Database of Systematic Reviews using the following key words and their related MeSh terms: “fluid challenge,” “fluid responsiveness,” “stroke volume variation,” “pulse pressure variation,” “dynamic indices OR indexes,” “passive leg raising,” “inferior cava vein collapsibility,” “systolic pressure variation.” Included papers were also examined to identify other studies of interest missed during the primary search.

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Data Extraction

Pairs of examiners evaluated sets of 15–16 articles. The 2 members of each pair, who performed the evaluation independently from each other, extracted from the selected articles the following information using an ad hoc standardized form: study setting (type of study, geographical area and time period where and when the study was performed, and sample size), patient sample characteristics (gender, age, reason for admission, underlying diseases, ICU scores of gravity, mode of ventilation, and inotropic/vasopressor support), and criteria for hemodynamic instability.

When data from specific studies were not available, the corresponding authors were contacted to obtain missing information. In case of disagreement between the 2 examiners, the opinion of a third, senior, examiner was requested for a conclusive decision (P.N. or G.S.). The list of excluded articles was reported in Supplemental Digital Content, http://links.lww.com/AA/B745. Results were overall summarized qualitatively, owing to the between-study clinical and methodological heterogeneity.

Patients were divided into subgroups for analysis according to the primary cause of hemodynamic instability. We divided patients into 4 groups defined as: (1) septic, ie, systemic inflammatory response syndrome, sepsis, and septic shock, or conditions determining systemic inflammation (ie, pneumonia, pancreatitis, and abdominal infections), (2) postsurgical (postoperative patients without additional complications), (3) cardiac (patients with cardiogenic shock or recovering after cardiac arrest), (4) hypovolemic (trauma, nontraumatic hemorrhagic conditions, dehydration).

We also assessed the relationship between rates of FC that exceeded the average response of the overall studies and primary reason for hemodynamic instability (see above); the 2 most common criteria for indicating FC administration; and modalities of FC delivery (type of fluid and rate of administration).

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Statistical Analysis

Statistical analysis was conducted on the summary statistics described in the selected articles (eg, means, medians, proportions) and, therefore, the statistical unit of observation for all the selected variables was the single study and not the patient. No meta-analyses on summary findings or on individual patient data were performed.

Descriptive statistics of individual studies used different statistical indicators for central tendency and variability, such as means and standard deviations (SD; ie, age, tidal volume, fluid responders, severity scores), whereas absolute and relative frequencies were adopted for qualitative variables. To show 1 single indicator for the quantitative variables we collected, means with SD or medians and interquartile ranges (IQR) were used, as appropriate.

Student t test or Mann-Whitney U test in case of parametric or nonparametric distributions, respectively, were used to assess a difference of mean values between responders and nonresponders.

A logistic regression was performed using summary statistics displayed in the selected articles with the scope of assessing the relationship between a proportion of responders higher than 52% (ie, average proportion of responders; we dichotomized the variable for the logistic regression purposes) and several independent covariates (ie, hemodynamic instability, oliguria, hypotension, type of fluid, and rate of administration).

The statistical software STATA13 (StataCorp, College Station, TX) was used to perform all the computations.

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RESULTS

Figure 1.

Figure 1.

The electronic search identified 870 potentially relevant studies. Detailed description of the selection process flow is provided in Figure 1. After evaluating 157 full-text manuscripts, the inclusion criteria were met by 71 studies, none published before 2000. Five of the 157 (3.1%) studies required revision by senior examiners because of disagreement between the coupled examiners. We did not find any further relevant publications by reviewing the bibliography of the selected studies.

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Study Design

Table 1.

Table 1.

Of the 71 studies included, 5 were multicentered (3 interventional9–11 and 2 observational12,13), while 64 were single-centered (45 prospective observational,14–58 19 prospective interventional,59–77 and 2 retrospective78,79 (Table 1). The median (IQR) of the mean duration of the studies was 9.0 (6.0–18.0) months; 60 of them (83.1%) were performed in a university hospital and 59 (81.7%) in European countries.

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Characteristics of the Population Enrolled

Overall, the 71 studies include 3617 patients, with a median (IQR) of 38 (31–59) per study. The median (IQR) of the mean patient age across studies was 61.0 (58.5–65.0) years overall, 25 (7–40) for patients with septic shock, 26 (16–32) for surgical 14 (7–18) for patients with cardiogenic shock, 6 (5–12) for patients with hypovolemic shock, 6 (4–11) for trauma patients, and 3 (2–5) for patients with hemorrhagic shock. The median (IQR) of the mean number of FCs administered was 39 (32–68).

Ten studies did not report gender.21,26,33,41,47,48,55,57,65,74 Thirty-two studies16–18,20–28,30,36–41,45,46,51,55,56,58–60,63,67,75,76,78 did not report any severity of illness scores at ICU admission. Of the remaining 39 studies, in 9 studies the median (IQR) of the mean reported sepsis-related organ failure assessment score was 10.5 (9.0–12.0),14,15,29,31,33,48–50,57 in 10 the median (IQR) of the mean reported acute physiology and chronic health evaluation score was 19.0 (17.0–23.0),15,29,47,50,61,66,69,70,77,79 and in 27 the median (IQR) of the mean a simplified acute physiology score was 55.0 (47.0–57.5).9–13,19,31,32,34,35,42–44,48,52–54,57,62,64–66,68,71–74,76

Twenty-four studies (33.8%) did not report the use of vasopressors or inotropes.9,15,16,18,20,26–28,32,36,47,48,55–58,63–65,68,70,76,77,79 In the remaining studies, norepinephrine was the most common (44/47, 93.6%), at a dose of 0.4 (0.2–0.7) µg/kg/min, followed by dobutamine (26/47, 55.3%), at 7.1 (6.0–8.0) µg/kg/min, dopamine (13/47, 27.7%) at 7.5 (5.0–10.0) µg/kg/min, and epinephrine (10/47, 21.3%) at 0.4 (0.15–0.55) µg/kg/min (median of the mean dose of drug reported across the studies).

The mode of ventilation was not specified in 10 (14.1%) studies,10,13,18,21,37,44,50,52,77,79 while 6 (8.5%) enrolled only spontaneously breathing patients.9,47,61,64,68,76 Thirty-nine (55.0%) studies included patients receiving volume-targeted controlled ventilation,11,12,15–17,19,20,22–26,28–31,34–36,38,41,45–48,51,53,54,56–58,65,67,69,70,72–74,78 with the median (IQR) of the mean tidal volume across studies of 7.4 (6.5–8.1) mL/kg. One (1.4%) included patients receiving pressure-targeted controlled ventilation.27 Two (2.8%) studies enrolled patients undergoing volume-targeted assist/control,33,71 1 (1.4%) pressure support,49 and 1 (1.4%) airway pressure release ventilation.14 The remaining studies enrolled a mixed population of patients spontaneously breathing or mechanically ventilated.32,40,42,43,59,60,62,63,75

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Indication for the Fluid Challenge

Several clinical, pharmacological, or laboratory indicators of fluid depletion were used to trigger a FC. Hypotension (systolic or mean arterial pressure either below a fixed value or expressed as percent reduction from baseline or a generic reduction of the blood pressure) was used in 48 (67.6%),9–13,17,19,20,23,25,28,29,31–36,38–45,47,48,50–54,56,59–61,63–65,68–72,74,76,77,79 oliguria (a drop in urine output below 0.5 mL/h for 2 or 3 consecutive hours) in 37 (52.1%),9–13,17,19,20,23,29,31,32,34,39–45,47,50,53,59–61,63,64,66,68–72,74,76,77,79 physician judgment in 35 (49.3%),9,13,15–17,19–26,29,31,33–35,37,40–44,56,57,59,67,69,71–75,77 clinical evidence of skin mottling in 33 (46.4%),10,12,13,17,19,20,23,29,31,32,39–45,47,50,59–61,63,64,68–72,74,76,77,79 tachycardia, as defined by an increase in heart rate above 100 to 110 beats/min, in 29 (40.8%),17,19,20,23,29,32,39–45,47,50,53,59–61,63,64,68–72,74,76,77 need for initiating or reducing administration of vasoactive drugs in 23 (32.3%),10–13,31,33–35,38–40,44,45,49,51,52,54,59,65,66,69,70,74 lactate increase in 17 (23.9%),10–13,19,20,32,34,41,44,47,49,50,65,72,74,79 diagnosis of sepsis/septic shock in 9 (12.7%),15,18,19,21,38,50,54,62,64 and renal or hepatic dysfunction in 5 (7.0%) studies (see Table 2).9,18–20,63

Table 2.

Table 2.

A safety limit interrupt the FC was used in 4 (5.6%) studies by the same authors.10–13

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Quantity of Fluid Challenge

Table 3.

Table 3.

In 12 (17%) studies,15,16,19–21,26,46,52–54,58,75 the median (IQR) of the mean volume administered was 7 (7–9) mL/kg. Of the remaining 59 (83.1%) studies, 55 (77.5%) infused 500 mL,9–14,17,22–25,27,29–45,47–51,55,56,59–74,76–78 2 (2.8%) 250 mL,18,28 1 (1.4%) 200 mL,57 and 1 (1.4%) 300 mL (see Table 3).79

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Type of Fluid Administered

Colloids were used in 44 (62.0%) studies, where 34 (77.3%) infused 6% hydroxyethylstarch,15,19–24,26,27,29,31,37–39,46–48,50,53–58,61,64,66–70,76,78,79 3 (6.7%) 4% succinyl-gelatine,35,51,52 and 2 (4.5%) 6%49 or 10% Dextran.28 In 5 (11.3%) studies, the type of colloid was unspecified.10–13,18 Twenty-six (36.5%) studies9,14,16,17,25,32–34,36,40–45,59,60,62,63,65,71–75,77 used crystalloids and 1 (1.5%) study utilized blood (Table 3).30

Figure 2.

Figure 2.

Of 6 studies identified in the 2000 to 2004 period, 5 (83.3%) infused colloids and another one (12.5%) blood. Of 27 studies in the 2005–2010 period, 18 (66.6%) used colloids and 9 (33.4%) crystalloids. Of 38 studies in the 2011 to 2014 period, 20 (52.5%) use colloids and 18 (47.5%) crystalloids (Figure 2).

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Duration of Fluid Administration

The duration of fluids administration was 30 minutes in 32 studies (45.1%),10–15,21,29,32,35,37–39,41,42,44,46,48–51,53,54,61,64,65,68–70,73–75 15 minutes in 15 studies (21.1%),9,17,19,22–24,26,30,47,52,60,63,66,67,77 20 minutes in 11 studies (15.5%),16,20,28,34,43,56,58,71,76,78,79 10 minutes in 9 studies (12.7%),25,31,33,36,45,57,59,62,72 and in 5,18 7.5,40 and 9055 minutes in one single study (1.4%). Only one study (1.4%) reported the infusion rate (10 mL/kg/h).27 The median (IQR) of the mean rate of infusion, across 58 studies indicating volume and duration of infusion, was 18 (6–67) mL/min (see Table 3).

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Hemodynamic Response

Overall, the mean (SD) of the mean rate of fluid responders across the studies was 52.0% (13.0%). Forty-four studies (62.0%) assessed fluid responsiveness considering the rate of increase in CI or CO. The positive response was defined by an increase ≥15% in 34 studies14–16,19–25,27,28,31,38,41–44,46,48,53,55,56,62,67,69,71–78; ≥10% in 7 studies10–13,49,50,79; ≥12% in 2 studies,44,59 and ≥11% in 1 investigation.46 Twenty-two (31.0%) studies utilized either SVI or SV for assessing fluid responsiveness; 15 of these studies considered positive response an increase ≥15%,17,18,29,32,34,35,37,39,58,60,61,63,64,68,70 5 studies ≥10%,33,36,51,52,57 and 2 single studies ≥12%65 and ≥ 5%.26 Five studies (7.0%) used aortic blood flow or aortic velocity-time integrals increase ≥15% to identify fluid responsiveness (see Table 3).40,45,47,59,66

Forty-five studies reported the variation of mean (SD) arterial pressure before and after FC, which was higher in responders than in nonresponders (11.5 ± 5.4% vs 6.1 ± 3.9%, respectively; P < .001).

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Subgroup Analysis

Only 2 subgroups of studies enrolled at least 75% of patients with one specific cause of hemodynamic instability, septic (31 studies12,15,19–21,27,29,33–35,37,38,41–44,49,50,54,60,62,64–66,68,70–73,76,78) and postsurgery (16 studies16,18,22–24,26,28,30,51,55–58,61,63,67). The median (IQR) of the mean rate of fluid responders did not differ between the 2 subgroups, 49% (42–49) and 59% (42–70) for septic and postsurgery, respectively (P = .27). Hypotension was the most common criteria for FC administration in both groups, (71.0% and 43.8% of septic and postsurgery subgroups, respectively). Oliguria was the second most used criteria for indicating FC, representing 58.1% and 12.5% of septic and postsurgery subgroup, respectively. Colloids were used in 19 (61.3%) of the 31 studies including predominantly septic patients, and in 13 (86.7%) of 16 studies of the postsurgery subgroup. The mean (SD) of the mean rate of fluid administration was 23.6 (11.2) mL/min in septic and 26.6 (11.9) mL/min in postsurgery. The median (IQR) of the mean duration of FC administration was 30 minutes (20–30) in septic and 15 minutes (15–20) in postsurgery (P = .02) subgroups.

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Assessment of Variables Affecting FC Outcome

Table 4.

Table 4.

Table 4 summarizes the logistic regression analysis assessing the relationship between the primary reasons determining hemodynamic instability (sepsis or postsurgical), presence of oliguria and hypotension (the 2 most common criteria for FC), rate of administration and a positive response rate exceeding the average rate (52%) of responders of the overall studies. We found no correlation between a higher rate of fluid responsiveness and any of these variables.

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DISCUSSION

In a systematic review of studies published in the last 20 years on the FC in critically ill adult patients, we found marked variability in the definition, implementation, and assessment of the FC. In the majority of the studies, a 500 cc bolus (most often of colloid) was infused over 30 minutes, without predetermined stopping rules, and ≥15% increases in CI or CO were used to assess the result. We also observed that the median time of FC administration and use of oliguria as a criterion for FC, were both more likely in the septic subgroup.

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Indication for the Fluid Challenge

The most common criteria for attempting a FC clinical signs such as hypotension (67.6% of studies) and oliguria (52.1% of studies) may not exclusively be the result of fluid depletion. For instance, ICU sedation affects both tachycardia and hypotension.80 Also, reduction in urinary output may result from renal dysfunction and thus not necessarily respond to a FC.81 Importantly, our subgroup analysis found oliguria to be more commonly used as an indication for FC in studies enrolling predominantly septic patients.

About half the patients in the studies we reviewed did not respond to fluid administration, which suggests that using these signs to identify potential fluid responders may not be successful.

Static or dynamic physiologic indices were utilized in a minority of studies (16.9%). This frequency is considerably less than the 57.3% reported by the FENICE study.8 The association between these indices and clinical signs may improve the selection of patients for FC. However, static indices, particularly central venous pressure are unreliable for fluid response assessment in ICU patients82 and pulse pressure variation, the most reliable dynamic index,83 can be properly used only in a small portion of ICU patients in whom all the validity criteria of this dynamic index are satisfied.84

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Quantity and Duration of Fluid Challenge

In 77.5% of the studies, the FC consisted of 500 mL fluid boluses. Five hundred milliliters was also the median volume FC used in the FENICE study.8 In 60.5% of studies, the infusion was administered in 20 or 30 minutes, with a median infusion rate of 18 mL/min, similar to the median 24 minutes and 17 mL/min recently reported by the FENICE study.8 Interestingly, the duration of volume administration was shorter in studies with a rate of FC responders ≥52%, suggesting that a more rapid FC may affect responsiveness. The phase of distribution among different tissue compartments for crystalloids normally takes 25–30 minutes, and the fraction remaining in the plasma is related to both duration and rate of infusion.85 Aya et al86 recently suggested an even shorter duration, finding that the hemodynamic effect of 250 mL of crystalloids infused over 5 minutes, is dissipated within 10 minutes, in both responders and nonresponders. The hemodynamic effect of colloids is likewise complex, as infusion of the same volume causes a greater plasma expansion in hypovolemic than in nonhypovolemic patients.87

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Type of Fluid Challenge

Figure 2 lists the type of fluids utilized for the FC throughout between 2000 and 2014. Overall, colloids were used more often than crystalloids. When grouping studies in 3 epochs, however, the ratio between colloids and crystalloids decreased from 5:0 in the 2000–2004 period, to approximately 3:1 in the 2005–2010 period, to approximately 1:1 in the 2011 to 2014 period. In keeping with this trend, a large 2007 cross-sectional study found colloids used more frequently than crystalloids,7 whereas in the 2013, FENICE survey crystalloids are more commonly used (74%).8

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Hemodynamic Response

While in 62.6% of the studies an increase of ≥15% of CI or CO immediately after FC completion defined a positive response, in current clinical practice fluid responsiveness is often assessed by an rise in arterial blood pressure.8 This metric only reflects an increase in CO in patients with high arterial elastance8 and is not reliable when used for passive leg raising test evaluation.88 The threshold value of the variable used to assess fluid responsiveness may thus influence the result of a FC for some patients, who may be responders when the threshold for responsiveness is 10% but nonresponders when the threshold is increased to 15%.

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CONCLUSIONS

The FC is not well standardized and lacks of consistency among the published studies. The most common form of administration, whose appropriateness remains to be clarified, consists in infusing 500 mL of crystalloid or colloids in 20 or 30 minutes, and assessing whether or not this infusion determines an increase in CI or CO ≥15%. Defining strict criteria for FC administration and response assessment is deemed necessary for meaningful comparisons of data among studies.

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DISCLOSURES

Name: Antonio Messina, MD, PhD.

Contribution: This author designed the study, collected the data, performed the data analysis, and wrote the manuscript.

Name: Federico Longhini, MD.

Contribution: This author helped with data collection, manuscript preparation, and data interpretation.

Name: Corinne Coppo, MD.

Contribution: This author helped with data collection, manuscript preparation, and data interpretation.

Name: Aline Pagni, MD.

Contribution: This author helped with data collection, manuscript preparation, and data interpretation.

Name: Ramona Lungu, MD.

Contribution: This author helped with data collection, manuscript preparation, and data interpretation.

Name: Chiara Ronco, MD.

Contribution: This author helped with data collection, manuscript preparation, and data interpretation.

Name: Marco Ambrogio Cattaneo, MD.

Contribution: This author helped with data collection, manuscript preparation, and data interpretation.

Name: Simone Dore, PhD.

Contribution: This author performed data analysis, helped with data interpretation, and manuscript preparation.

Name: Giovanni Sotgiu, MD.

Contribution: This author performed data analysis, helped with data interpretation, and manuscript preparation.

Name: Paolo Navalesi, MD, FERS.

Contribution: This author designed the study, collected the data, performed the data analysis, and wrote the manuscript.

All authors listed on the title page have read the draft, confirmed the validity and legitimacy of the data and its interpretation, approved the final version, and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

This manuscript was handled by: Avery Tung, MD, FCCM.

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