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REVIEW

CURRENT
OPINION Assessment of fluid responsiveness:
recent advances
Xavier Monnet a and Jean-Louis Teboul b

Purpose of review
In the field of prediction of fluid responsiveness, the most recent studies have focused on validating new
tests, on clarifying the limitations of older ones, and better defining their modalities.
Recent findings
The limitations of pulse pressure/stroke volume variations are numerous, but recent efforts have been made to
overcome these limitations, like in case of low tidal volume ventilation. Following pulse pressure/stroke
volume variations, new tests have emerged which assess preload responsiveness by challenging cardiac
preload through heart–lung interactions, like during recruitment manoeuvres and end-expiratory/inspiratory
occlusions. Given the risk of fluid overload that is inherent to the ‘classical’ fluid challenge, a ‘mini’ fluid
challenge, made of 100 ml of fluid only, has been developed and investigated in recent studies. The reliability
of the passive leg raising test is now well established and the newest publications have mainly aimed at
defining several noninvasive estimates of cardiac output that can be monitored to assess its effects.
Summary
Research in this field is still very active, such that several indices and tests of fluid responsiveness are now
available. They may contribute to reduce excessive fluid balance by avoiding unnecessary fluid
administration and, also, by ensuring safe fluid removal.
Keywords
cardiac output, fluids, passive leg raising, preload responsiveness, volume expansion

INTRODUCTION cardiac output to a fluid bolus. Nevertheless, the

As it has become clear that patients with circulatory
failure inconstantly respond to volume expansion
by increasing cardiac output [1], a whole vein of
intensive care research has been dug to develop tests
that predict ‘fluid responsiveness’ [2]. This gold rush
has been greatly enhanced by the growing evidence
that fluid overload is deleterious in critically ill
patients, especially with acute respiratory distress
syndrome (ARDS) and septic shock [3 ]. The most
&&
recent recommendations in septic shock suggest
managing the fluid strategy by using these
‘dynamic’ tests of fluid responsiveness [4].
Research in this field remains very active: develop-
ment of new tests, more precise definition of the lim-
itations of the older ones, invention of means to
circumvent these limitations, better description of the
tests methodology. We will review these advances in
this review of the most recent literature.
FLUID CHALLENGE: LARGE, MEDIUM, OR
SMALL?
The most intuitive way to test if the heart is sensitive
to preload changes is to observe the response of
‘traditional’ fluid challenge poses two problems.
On the one hand, to judge its effects, it is necessary
to measure or estimate cardiac output directly
as changes in blood pressure (BP) during a bolus
of fluid are partially [5] or totally [6] unable to
detect the response in terms of cardiac output. On
the other hand, the method, which involves
the irreversible administration of the treatment
itself, intrinsically entails a fluid overload if it
is repeated.
To circumvent this latter problem, some authors
have developed a ‘mini’ fluid challenge with 100 ml
of starch only (Table 1). They showed that the
response to a subsequent volume expansion
a
Service de réanimation médicale, AP-HP, Hôpital de Bicêtre and
b
Inserm, UMR S_999, Univ Paris-Sud, Le Kremlin-Bicêtre, France
Correspondence to Prof. Xavier Monnet, Service de réanimation méd-
icale, Hôpital de Bicêtre, 78, rue du Général Leclerc, 94 270 Le Kremlin-
Bicêtre, France. Tel: +33 1 45 21 35 47; fax: +33 1 45 21 35 51;
e-mail: xavier.monnet@ aphp.fr
Curr Opin Crit Care 2018, 24:000–000
DOI:10.1097/MCC.0000000000000501

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Cardiopulmonary monitoring

analysis, which provides a very accurate measure-

KEY POINTS
 To avoid the fluid overload that may appear in case of
repeated ‘classical’ fluid challenges, a ‘mini’ fluid
challenge could be used to assess fluid responsiveness.
It likely requires a precise measurement of
cardiac output.
 The PLR test, which reliability has been well established,
must be performed with a continuous and real-time
cardiac output measurement. The techniques that have
been well established for this purpose include
echocardiography, pulse contour analysis,
oesophageal Doppler, and changes in end-tidal carbon
dioxide in ventilated patients.
 The EEO requires that the patient tolerates a hold of
ventilation of at least 15 s, and that the measurement of
cardiac output is precise.
 Observing the decrease in cardiac output during
recruitment manoeuvres is likely an interesting way to
test fluid responsiveness in ventilated patients.
(500 ml) was predicted by the increase in velocity
time integral (VTI) of the left ventricular outflow
tract, a reflection of stroke volume measured by
echocardiography, induced by the infusion of this
small amount of fluid [7].
In our opinion, the main limitation of the ‘mini’
fluid challenge is that it induces only small changes
in cardiac output so that the technique used to
measure these changes must be very precise
(Table 1). In this regard, echocardiography is proba-
bly not the most appropriate tool. Pulse contour
ment of cardiac output [8], is likely more appropri-
ate [9,10].
It has been suggested that the prediction of the
response to volume expansion was less good when
not 100 but 50 ml was used to practice fluid flush [9].
This suggests that the volume is too small to gener-
ate sufficient preload changes to test preload respon-
siveness. The minimum volume of fluid to cause a
significant haemodynamic effect has been demon-
&
strated to be 4 ml/kg [11 ]. Finally, not only the
volume of fluid but also the timing of administra-
tion is important to consider. It has been recently
shown that the longer the duration of the fluid
challenge, the lower the proportion of fluid
responders [12].
PASSIVE LEG RAISING TEST: NEW WAYS
TO MEASURE ITS EFFECTS?
Many studies have shown that the transfer of a
patient from the semirecumbent position to a posi-
tion where the trunk is horizontal and the lower
limbs raised to 458, causes a transfer of venous blood
sufficient to increase the cardiac preload and to test
preload responsiveness. The reliability of the passive
leg raising (PLR) test has been established today
&
[13 ]. The last version of the Surviving Sepsis Cam-
paign recommends to use the PLR test as a ‘dynamic’
measure for guiding the fluid strategy during septic
shock [4]. The advantage of the test is that it can be
used in many circumstances where pulse pressure
variation (PPV)/stroke volume variation (SVV) are
not valid, such as spontaneous breathing, cardiac

Table 1. Summary of methods predicting preload responsiveness with diagnostic threshold and limitations

Method Variable Threshold Main limitations

Pulse pressure/Stroke volume Pulse pressure or 12% Cannot be used in case of spontaneous breathing, cardiac
variations stroke volume arrhythmias, low tidal volume/lung compliance
Inferior vena cava diameter Diameter 12% Cannot be used in case of spontaneous breathing, low tidal
variations volume/lung compliance
Superior vena cava diameter Diameter 36%a  Requires performing transoesophageal Doppler
variations  Cannot be used in case of spontaneous breathing, low tidal
volume/lung compliance
Passive leg raising Cardiac output 10% Requires a direct measurement of cardiac output
End-expiratory occlusion test Cardiac output 5%  Cannot be used in nonintubated patients
 Cannot be used in patients who interrupt a 15-s respiratory
hold
‘Mini’-fluid challenge (100 ml) Cardiac output 6%b Requires a precise technique for measuring cardiac output
‘Conventional’ fluid challenge Cardiac output 15%  Requires a direct measurement of cardiac output
(500 ml)  Induces fluid overload if repeated
Tidal volume fluid challenge Pulse pressure variation 3.5% Requires a precise technique for measuring cardiac output

a
Thresholds from 12 to 40% have been reported.
b
10% is more compatible with echography precision. Citations indicate the most important reference regarding the test.

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MCC 240310
arrhythmias, and ventilation with a low tidal vol-
ume or low pulmonary compliance [14–16]. The
test must be performed respecting a few simple
but essential rules [17].
One of the limitations of the PLR test is that it
cannot be performed in some circumstances like
during surgical interventions or in patients during
prone positioning (Table 1). In the latter circum-
stance, replacing PLR by a Trendelenburg manoeuvre
has been interestingly described [18]. The main limi-
tation of PLR is that it requires a direct measurement
of cardiac output [17]. BP changes are not reliable
enough to estimate the stroke volume changes
&
induced by PLR [13 ]. In addition, this measurement
of cardiac output must detect changes in cardiac
output in real time to capture the maximum effects
of the PLR test, which occur within seconds and
vanish after 1 min in some patients [19]. Pulse con-
tour analysis, calibrated or not, is suitable. Oesopha-
geal Doppler was used from the first studies validating
the test [19]. Changes in VTI measured by echocardi-
ography have been used in many studies [20].
Recently, several investigations have explored
other estimates of cardiac output, especially nonin-
vasive, that can be used. Some of them have sug-
gested that the PLR test can be performed by
measuring changes in blood velocity in the femoral
or carotid arteries [21], even if opposite results have
been reported [22]. The cardiac output estimated
from pulse contour analysis of a volume clamp-
derived BP seems accurate [23]. It was reported a
few years ago that the bioreactance technique
was not reliable to measure the PLR effects [24].
In fact, this device averaged cardiac output over a
period of 30 s, that is, not in real time. Nevertheless,
the most recent version of the Starling-SV system,
which averages cardiac output over only 8 s, makes
it possible to assess the effects of the PLR
quite correctly [25]. Changes in end-tidal carbon
dioxide, which are proportional to changes in car-
diac output, are a completely noninvasive method
of interest [26,27], even though they can only be
used in intubated patients perfectly adapted to
the ventilator.
NEW TESTS USING HEART–LUNG
INTERACTIONS
Following PPV and SVV, newer tests use cardiac
preload changes induced by mechanical ventilation
to detect preload responsiveness.
Respiratory occlusion tests
The end-expiratory occlusion (EEO) test, developed
a few years ago [28], consists of interrupting
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Fluid responsiveness Monnet and Teboul
mechanical ventilation for 15 s at and expiration
and observing changes in cardiac output. If this
increases by more than 5%, the test is positive,
and the patient is most likely preload responsive
[28]. The initial findings have been recently con-
&
firmed with a 30-s EEO test [29 ].
In fact, the test is based on the premise that
when ventilation is stopped at expiration, the cyclic
impediment in venous return caused by each insuf-
flation is interrupted. This leads to an increase in
right cardiac preload. The duration of interruption
(15 s) is sufficient to allow the resulting increase in
right ventricular stroke volume (in case of preload
responsive right ventricle) to cross the pulmonary
circulation and in turn increase the left cardiac
preload. This is an effective preload challenge for
both ventricles. The essential limit is that it cannot
be used in patients whose respiratory activity does
not allow a 15-s hold without interrupting it
(Table 1).
As with the PLR test, the question arises as to
whether less invasive techniques for measuring car-
diac output are reliable enough to perform the EEO
test. Recently, our team has shown that changes in
VTI measured by echocardiography allow the EEO
&
test to be monitored reliably [30 ]. However, the
diagnostic threshold was an increase in VTI of 4%.
As discussed earlier, the precision of echocardiogra-
phy is insufficient for reliably detecting so small
changes. That is why, to the 15-s EEO, we added a
15-s end-inspiratory occlusion (EIO), which lowered
cardiac output more in preload-dependent patients
than in others. When the absolute value of the
changes in VTI induced by the successive EEO
and EIO were added, they predicted fluid respon-
siveness with a reliability identical to the EEO
alone, but with a diagnostic threshold of 15%
&
[30 ]. This is much more consistent with the preci-
sion of echocardiography. It is a likely that in the
coming years, studies will explore other techniques
to measure the effects of the respiratory occlusions
tests.
Recruitment manoeuvres
It has been quite recently that the hemodynamic
effects of these manoeuvres have been studied as a
&
preload responsiveness test [31,32 ]. In principle,
the increase in intrathoracic pressure induced by
recruitment manoeuvres is transmitted to the right
atrium, decreasing cardiac preload. Preload respon-
siveness of both ventricles is tested by measuring
the resultant changes in cardiac output. However,
the haemodynamic effect of these manoeuvres may
be ambiguous because the increase in alveolar pres-
sure also increases the transpulmonary pressure, the
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Cardiopulmonary monitoring
effect of which is to increase pulmonary vascular
resistance and right ventricular afterload.
The published studies, for the moment few, are
&
in favour of the reliability of the test [31,32 ]. It is
interesting to note that, in preload independent
patients, stroke volume also decreased, albeit to a
&
lesser extent than in others [32 ]. This suggests that a
mechanism different from the preload decrease, like
the increase in right ventricular afterload, inter-
venes during recruitment manoeuvres. This suggests
at the very least that more studies are needed to
validate the test, which will only be intended for
patients in the operating room or with the most
severe ARDS.
PULSE PRESSURE VARIATION AND
STROKE VOLUME VARIATION: CLEVER
WAYS TO CIRCUMVENT THE LIMITATIONS
These indices of preload responsiveness, the first
that have been developed, are those based on the
highest level of evidence [2]. Nevertheless, it is also
those with the most restrictive conditions of valid-
ity. The circumstances generating false positives and
false negatives of PPV and SVV are numerous, espe-
cially in critically ill patients.
Among these circumstances, mechanical venti-
lation with a low tidal volume is one of the most
common (Table 1). To circumvent this limit, a ‘tidal
&
volume challenge’ has been developed [33 ], which
consists in increasing tidal volume from 6 to 8 ml/kg
for a few minutes. If PPV increases at least 3.5% (in
absolute value) during the test, preload responsive-
&
ness is likely [33 ]. The test has the advantage of not
requiring a direct measurement of cardiac output
[34]. Sometimes, even during normal tidal volume
ventilation, it can be difficult to interpret PPV,
when its value lies in a zone of uncertainty (between
9 and 13%) described by Cannesson et al. as a [35]
‘gray zone’. A recent study showed that in such a
situation, the increase in PPV predicted fluid
responsiveness when tidal volume was increased
&
from 8 to 12 ml/kg [36 ].
It should be kept in mind that during ARDS,
the false negatives encountered for PPV and SVV
are explained not only by the low tidal volume but
also by the decreased lung compliance [37,38].
Another way to circumvent the limitation of PPV
in case of low tidal volume that has been investi-
gated consisted in indexing it with the changes
in pleural pressure, assessed by an oesophageal
catheter [38]. The method performs much
better than indexation by tidal volume. Neverthe-
less, this method requires an oesophageal pressure
catheter in place, what is still uncommon at the
bedside.
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Another way to use PPV in circumstances gen-
erating false positives and false negatives would be
to use it instead of cardiac output to judge the effects
of a preload challenge. One study showed that the
decrease in PPV during a PLR test predicted the
response to volume expansion as well as concurrent
changes in cardiac output. Nevertheless, these
results are questioned by a recent study showing
that PPV did not track the changes in cardiac output
during a fluid challenge [39].
RESPIRATORY VARIATION OF THE VENA
CAVA DIAMETER: REALLY RELIABLE?
Regarding these indices, recent publications espe-
cially lead us to question reliability. Some of the
studies validating the collapsibility of the inferior or
superior vena cava diameter found disappointing
results, so that a meta-analysis reported a prediction
that was globally acceptable but far from perfect
&
[40 ].
In addition, a recent large-scale study found a
moderate predictive value of both variabilities of
&
superior and inferior vena cava diameter [41 ], far
lower than in previous studies. This casts doubt on
the reliability of these indices. Nevertheless, it
should be noted that even PPV provided a poor
prediction of preload responsiveness. This suggests
that the indices and tests of preload responsiveness
were not carried out with sufficient rigor in this
&
‘real-life’ study [41 ].
The respiratory variation of vena cava diameter
shares with PPV and SVV that it cannot be used in
case of low tidal volume and spontaneous breath-
ing. Nevertheless, a recent study reported that the
changes in inferior vena cava diameter induced by a
deep standardized inspiration in nonintubated
patients provided a good prediction of fluid respon-
siveness [42]. The idea of using the respiratory
variation of the diameter not of vena cava but of
the internal [43] or subclavian [44] veins, which has
very recently emerged, should be more thoroughly
investigated.
NOBODY IS PERFECT!
None of the indices of preload responsiveness has
shown to predict fluid responsiveness with absolute
sensitivity and specificity. Moreover, the interpreta-
tion of these tests has an intrinsic limit. For the
purpose of statistical analysis, the status of fluid
responsiveness has been dichotomously described:
present or absent. In fact, the response to fluid
administration is conventionally defined by an
increase in cardiac output of more than 15%,
whereas it is a continuous variable. Is a patient with
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MCC 240310
a 14% increase so different from another in whom
fluid increases cardiac output by 16%? In practice,
this limit must be taken into account at the
bedside. The predictive certainty is all the more
established as the observed changes are remote from
the diagnostic threshold.
It is the advantage of having at our disposal
today many of these tests [2]. In patients for whom
it is considered necessary crucial to detect preload
responsiveness or unresponsiveness, for example
in patients with circulatory failure and ARDS, one
should use several tests when the response of
cardiac output is close to thresholds described by
the literature.
Finally, a reasoned fluid strategy should not be
based only on fluid responsiveness indices. The
decision to administer fluid should also take into
account the risk of fluid administration. It should be
evaluated for instance on the degree of lung
impairment, the level of extravascular lung water
[45], or of the left ventricular filling pressure. The
relative weight of this risk must be compared with
the advantage of increasing cardiac output.
CONCLUSION
The literature devoted to the tests and indices of
preload responsiveness has been abundant and a
review like this one can obviously not report it
entirely. These markers are now available at the
bedside to make sure that the volume expansion
that one is about to perform will be effective. They
are even more useful for detecting preload unre-
sponsiveness, avoiding unnecessary and dangerous
fluid administration. Although limited for the
moment, there are today some studies telling us
that using these tests reduce fluid administration
in critically ill patients [46,47]. A recent meta-anal-
ysis even suggested that it may decrease mortality
[48]. They are helpful for guiding fluid administra-
tion but also for guiding fluid removal, which can be
safely performed when tests have verified that there
&
is no preload responsiveness [49 ,50].
Acknowledgements
None.
Financial support and sponsorship
None.
Conflicts of interest
Professors X.M. and J.L.T. are members of the Medical
Advisory Board of Pulsion Medical Systems, member of
Getinge. They gave lectures for Cheetah Medical and for
Masimo.
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Fluid responsiveness Monnet and Teboul
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