AJRCCM Articles in Press. Published on February 13, 2003 as doi:10.1164/rccm.

200203-195OC

Prevention of Endotracheal Suctioning-induced Alveolar Derecruitment in Acute Lung

Injury

Salvatore M. MAGGIORE1, Franois LELLOUCHE2, Jrme PIGEOT2, Solenne TAILLE2,

Nicolas DEYE2, Xavier DURRMEYER2, Jean-Christophe RICHARD3, Jordi MANCEBO4,
Franois LEMAIRE2, Laurent BROCHARD2
1

Department of Anesthesiology and Intensive Care, Agostino Gemelli Teaching Hospital,

Universit Cattolica del Sacro Cuore, Rome, Italy;

Medical Intensive Care Unit, INSERM

U492, Henri Mondor Teaching Hospital, AP-HP, Paris XII University, Crteil, France;

Medical Intensive Care Unit, Charles Nicolle Teaching Hospital, Rouen, France; 4 Servei de
Medicina Intensiva, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain

Send all correspondence including reprint requests to:

Prof. L. Brochard, Ranimation Mdicale, Hpital Henri Mondor, 94000 Crteil, France.
Phone: +33 1 49 81 23 92; Fax: +33 1 42 07 99 43;
E-mail: [email protected]

This study was supported by INSERM U492. The equipment was kindly furnished by TYCO
Healthcare, CA, USA.
Running Title: Endotracheal Suctioning in Acute Lung Injury
Descriptor numbers: 2 - 10 -13
Word count (text without abstract and references): 4128
This article has an online data supplement, which is accessible from this issues table of
content online at www.atsjournals.org

Copyright (C) 2003 by the American Thoracic Society.

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ABSTRACT

We studied endotracheal suctioning-induced alveolar derecruitment and its prevention

in nine patients with acute lung injury. Changes in end-expiratory lung volume measured by
inductive plethysmography, PEEP-induced alveolar recruitment assessed by pressure-volume
curves, oxygen saturation, and respiratory mechanics were recorded. Suctioning was
performed after disconnection from the ventilator, through the swivel adapter of catheter
mount, with a closed system, and with the two latter techniques while performing recruitment
maneuvers during suctioning (40 cmH2O pressure-supported breaths). End-expiratory lung
volume after disconnection fell more than with all other techniques (-1466586, -733406, 531228, -168176 and -284317 ml after disconnection, through the swivel adapter, with
the closed system, and with the two latter techniques with pressure-supported breaths,
respectively, p<0.001), and was not fully recovered 1-min after suctioning. Recruitment
decreased after disconnection and using the swivel adapter (-10431 and -6325 ml,
respectively), was unchanged with the closed system (-110 ml), and increased when
performing recruitment maneuvers during suctioning (7137 and 6030 ml) (p<0.001).
Changes in alveolar recruitment correlated with changes in lung volume (rho=0.88, P<0.001)
and compliance (rho=0.9, P<0.001). Oxygenation paralleled lung volume changes.
Suctioning-induced lung derecruitment in acute lung injury can be prevented by performing
recruitment maneuvers during suctioning and minimized by avoiding disconnection.

Word count: 199

Key words: endotracheal suctioning, alveolar recruitment, closed suctioning system,
recruitment maneuver, acute lung injury

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INTRODUCTION

It has been suggested that ventilator associated lung injury can be caused by high
transpulmonary pressures at the end of inspiration and/or insufficient recruitment at the end of
expiration, in patients with acute lung injury (ALI) and acute respiratory distress syndrome
(ARDS) (1). Preventing alveolar overdistension and derecruitment are the goals of recently
proposed protective ventilatory strategies. In this context, the periodic derecruitment induced
by endotracheal suctioning could be harmful in ALI/ARDS patients. In addition, the
application of a subatmospheric pressure generates alveolar injury in case of surfactant
dysfunction (2). Most of the studies on endotracheal suctioning have concentrated on
reversing or preventing hypoxemia resulting from such a procedure. Few data exist about the
effect of endotracheal suctioning on lung volumes (3-5), and no study has assessed the
consequences of suctioning on alveolar recruitment in ALI/ARDS. In patients with various
etiologies of acute respiratory failure, Brochard et al. demonstrated that one major mechanism
causing hypoxemia during suctioning was the decrease in lung volume induced by the loss of
positive alveolar pressure. This phenomenon could be prevented by the use of continuous
oxygen insufflation via a special endotracheal tube generating a positive pressure during
suctioning (3). The need to use a modified endotracheal tube, however, limits the clinical
application of this technique. Recently, Cereda et al. reported that using a closed suctioning
system allowed to prevent partially the fall of end-expiratory lung volume and hypoxemia
observed when endotracheal suctioning was performed after disconnection from the
ventilator, in patients with ALI (4). The effect of the closed system on the recruitment induced
by positive end-expiratory pressure (PEEP) was not studied. Lately, Lu et al. have shown that
a recruitment maneuver performed after endotracheal suctioning could reverse atelectasis
resulting from such a procedure, in an animal model (5). However, the prevention of the

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endotracheal suctioning-related lung volume loss could be more clinically relevant (6, 7). In
addition, whether a better prevention could be obtained by the use of special maneuvers
during suctioning needed to be studied.
The aims of our study were: 1) to assess the magnitude of lung volume fall during
endotracheal suctioning and determine the respective roles of PEEP loss and negative
pressure, 2) to assess the impact of endotracheal suctioning performed with different
techniques on alveolar recruitment/derecruitment in patients with ALI/ARDS, and 3) to try to
prevent derecruitment by performing a special recruitment maneuver during endotracheal
suctioning. We hypothesized that such a maneuver could prevent the alveolar derecruitment
and the decrease in oxygenation. The effect of different suctioning techniques on lung
volumes, alveolar recruitment/derecruitment, arterial oxygenation and respiratory mechanics
was assessed and compared in nine patients with ALI/ARDS.

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METHODS (word count = 499)

Patients
The institutional ethics committee approved the protocol. Written informed consent
was obtained from the patients next of kin. Patients fulfilling criteria for ALI/ARDS (8) were
eligible. Patients were not included in case of a leaking chest tube, contraindication to
sedation or paralysis, and respiratory or hemodynamic instability over the last 6 hours. Nine
patients were studied (Table 1).
Patients were sedated, paralyzed and mechanically ventilated in volume-controlled
mode. All had an 8.0-mm endotracheal tube. Tidal volume was 6-8 mlkg-1, respiratory rate
was 18-25 min-1, PEEP was chosen by the attending physician. The inspired oxygen
concentration was set to have pulse-oximeter oxygen saturation (SpO2) 92%.

Measurements
Changes in end-expiratory lung volume were measured by inductive plethysmography,
as previously described (9). The end-expiratory lung volume change was calculated as the
difference between the volumes measured at the end of expiration just before and at the end of
each suctioning procedure (Figure 1). Lung volume change was also measured following
suctioning, at the first breath after resuming baseline ventilation and after one minute, before
elastic pressure-volume (Pel-V) curves recording.
Pel-V curves from PEEP and from the static equilibrium volume at zero end-expiratory
pressure (ZEEP) were acquired before and one minute after each suctioning procedure, using
the low sinusoidal flow technique, as described (10, 11). Linear compliance at ZEEP and
PEEP-related alveolar recruitment/derecruitment at the elastic pressure of 20 cmH2O were
measured (10-15).

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SpO2 changes were calculated as the difference between the value before suctioning
and the minimum value recorded up to one minute after each suctioning procedure.
Signals were recorded and stored in a computer for subsequent analysis.
Details on measurement of end-expiratory lung volume, Pel-V curve, alveolar
recruitment, airway pressures and respiratory resistance are given in the online supplement.

Protocol (see details in online supplement)

A flow-chart of protocol and measurements is shown in Figure 2. Endotracheal
suctioning was performed:
1) after disconnection from the ventilator (DISCONNECTION);
2) without disconnection, introducing the suction catheter through the swivel adapter of the
catheter mount (SWIVEL);
3) with a closed suctioning system (CLOSED) (Hi-Care; Tyco Healthcare, CA, USA);
4) during SWIVEL, while triggering pressure-supported breaths at a peak inspiratory
pressure of 40 cmH2O during suctioning (SWIVELPSV );
5) during CLOSED, while triggering 40 cmH2O pressure-supported breaths during
suctioning (CLOSEDPSV) (Figure 1).
Trigger function was inhibited during procedures 1 to 3 and was set at 1 cmH2O during
phases 4 and 5. Suctioning techniques were performed in random order and were separated by
at least 30 min. The suction catheter (Fr 14) was inserted into the airways until resistance was
met and then pulled back 2 cm. Intermittent suctioning was started while the catheter was
gradually removed. Each suctioning maneuver lasted 25-30 seconds. Negative pressure was
set at 200 cmH2O.

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Statistics
Results are reported as meanSD. Comparison of suctioning techniques was made by
analysis of variance (Friedman test), and two-by-two comparisons were made using the
Wilcoxon test for paired samples. Regression analysis (Spearman rho) was used when
required. P<0.05 was considered statistically significant.

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RESULTS

End-expiratory lung volume

These data are shown in Figures 1 and 3, and Table 2. End-expiratory lung volume
decreased during endotracheal suctioning, whatever the technique. The largest end-expiratory
lung volume fall was observed with DISCONNECTION, and it was significantly different
from SWIVEL and CLOSED (-1466 586, -733 406 and -531 228 ml, respectively,
P<0.001). The drop of end-expiratory lung volume during suctioning was minimal with
SWIVELPSV and CLOSEDPSV (-168 176 and -284 317 ml, respectively, P=NS), and
significantly smaller (P<0.001) than with the three other techniques without pressuresupported breaths. When suctioning was performed with DISCONNECTION, the simple
disconnection from the ventilator and the application of negative pressure contributed equally
to the total end-expiratory lung volume drop (728 377 ml and 737 383 ml, respectively).
However, large variations existed in the individual patients: in some patients, disconnection
alone contributed the most while, in others, suctioning was the main determinant of the total
loss of lung volume (Figure 1). A correlation between the level of external PEEP and the fall
in lung volume observed after disconnecting patients from the ventilator, before suctioning,
was found: the higher the external PEEP, the higher the lung volume drop observed after
disconnection alone, before applying the negative pressure (rho = 0.7, P<0.05). One breath
after resuming normal ventilation, the residual lung volume loss was still large after
DISCONNECTION, while it was minimal after SWIVEL and CLOSED (-1116 460, -276
310 and -122 101 ml, respectively, P<0.001). One breath after SWIVELPSV and
CLOSEDPSV, the minimal drop of end-expiratory lung volume observed during endotracheal
suctioning was completely recovered (7 136 and -16 86 ml, respectively, P<0.001
compared to the other techniques). One minute after endotracheal suctioning, just before Pel-V

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curves recording, the end-expiratory lung volume was still not fully recovered with
DISCONNECTION, while it was almost totally restored with both SWIVEL and CLOSED
and increased with both SWIVELPSV and CLOSEDPSV (-278 239, -89 58, -44 53, 93
53 and 64 38 ml, respectively, P<0.001).

PEEP-induced alveolar recruitment

Pressure-volume curves obtained from ZEEP and from PEEP and the quantification of
alveolar recruitment, before and after the different suctioning techniques, in a representative
patient (#4) are shown in Figure 4.
PEEP-induced alveolar recruitment decreased in all patients one minute after
endotracheal suctioning with both DISCONNECTION and SWIVEL (239 114 ml before vs
135 101 ml after suctioning with DISCONNECTION, P<0.01, and 236 111 ml vs 173
92 ml with SWIVEL, P<0.01) (Figure 5). Alveolar recruitment did not change after
endotracheal suctioning performed with a closed system (233 114 ml before vs 232 113
ml after suctioning, P=NS), while it increased when endotracheal suctioning was performed
while triggering pressure-supported breaths (232 110 ml before vs 303 108 ml after
suctioning with SWIVELPSV, P<0.01, and 233 110 ml vs 294 109 ml with CLOSEDPSV,
P<0.01) (Figure 5). The changes in alveolar recruitment correlated with the end-expiratory
lung volume variations observed during endotracheal suctioning (rho = 0.68, P<0.001), one
breath after suctioning (rho = 0.75, P<0.001), and one minute after suctioning (rho = 0.88,
P<0.001) (Figure 6).

Arterial oxygen saturation

Data on arterial oxygen saturation were not available for patient #2. In eight patients,
SpO2 values before the different suctioning techniques were identical (96.1 2.8, 96.2 2.9,

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95.7 2.2, 96.2 2.7 and 96.1 2.2 % before DISCONNECTION, SWIVEL, CLOSED,
SWIVELPSV and CLOSEDPSV, respectively, P=NS). As shown in Figure 7, SpO2 decreased
with all the techniques used. However, the drop in SpO2 was much greater when endotracheal
suctioning was performed after the disconnection from the ventilator than with all the other
techniques (-9.2 7.6, -1.7 0.9, -2.2 2.7, -1.5 0.6 and -1.3 0.6 % with
DISCONNECTION, SWIVEL, CLOSED, SWIVELPSV and CLOSEDPSV, respectively,
P<0.01). The decrease in SpO2 correlated with the changes in alveolar recruitment (rho =
0.44, P<0.01) and the changes in end-expiratory lung volume during endotracheal suctioning
(rho = 0.43, P<0.01), one breath after suctioning (rho = 0.53, P<0.001) and one minute after
endotracheal suctioning (rho = 0.46, P<0.01).

Respiratory system mechanics

Pressure at the lower inflection point of the Pel-V curve from ZEEP decreased, albeit
not significantly, after DISCONNECTION (P=0.06), it did not change after SWIVEL and
CLOSED, while it increased significantly after SWIVELPSV (P<0.05) and tended to increase
after CLOSEDPSV (P=0.06) (Table 3 and online data supplement). Similarly, the volume at
the lower inflection point of the Pel-V curve from ZEEP tended to decrease after
DISCONNECTION (P=0.06), increased significantly after SWIVELPSV (P<0.05), while it did
not change with the other techniques (Table 3 and online data supplement).
Compliance of the first segment of the pressure-volume curve from ZEEP, below the
lower inflection point, decreased significantly after DISCONNECTION (P<0.05). It increased
after SWIVELPSV (P<0.05), while it did not change with the other techniques (Table 3 and
online data supplement). Compliance of the linear segment of the Pel-V curve from ZEEP,
above the lower inflection point, decreased after both DISCONNECTION (P<0.01) and
SWIVEL (P<0.01), while it did not change after CLOSED, and even increased when

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endotracheal suctioning was performed while triggering pressure-supported breaths (P<0.01)
(Table 3 and online data supplement). The changes in linear compliance correlated with the
changes in end-expiratory lung volume one minute after endotracheal suctioning (rho = 0.84,
P<0.001), with the changes in alveolar recruitment (rho = 0.90, P<0.001) (Figure 8), and with
the changes in oxygen saturation (rho = 0.47, P<0.01).
Peak airway pressure increased, albeit not significantly, after DISCONNECTION and
SWIVEL. It did not change with CLOSED, and decreased significantly after SWIVELPSV and
CLOSEDPSV (P<0.01) (Table 3).
End-inspiratory plateau pressure decreased significantly after CLOSED (P<0.05),
SWIVELPSV (P<0.05) and CLOSEDPSV (P<0.01), while it did not change with the other
techniques (Table 3).
Total respiratory resistance increased significantly after DISCONNECTION (P<0.05)
and SWIVEL (P<0.05), suggesting that endotracheal suctioning could have induced
bronchoconstriction. It tended to increase with CLOSED (P=0.06), while it did not change
after SWIVELPSV and CLOSEDPSV (Table 3).

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DISCUSSION

The main results of this study can be summarized as follows: 1) the drop in lung
volume observed during endotracheal suctioning resulted from both the loss of PEEP and the
application of a negative pressure; 2) avoiding disconnection during suctioning partially
avoided a large fall in lung volume, while performing a recruitment maneuver during
suctioning fully prevented a lung volume drop; 3) PEEP-induced recruitment decreased with
any suctioning techniques requiring the opening of ventilator circuit, but could be preserved
by using a closed system, and increased when performing a recruitment maneuver during
suctioning; 4) changes in arterial oxygen saturation paralleled changes in end-expiratory lung
volume, and oxygen saturation was virtually unaffected by endotracheal suctioning when the
drop in lung volume was avoided; 5) endotracheal suctioning-induced increase in airway
resistance was small and fully prevented by performing a recruitment maneuver during
suctioning.

Endotracheal suctioning-induced changes in end-expiratory lung volume

Endotracheal suctioning performed after disconnection from the ventilator may induce
a large lung volume drop and alveolar collapse, particularly in ALI/ARDS patients ventilated
with PEEP (4, 16). Indeed, endotracheal suctioning with disconnection induced almost 1.5 L
volume loss (Figures 1 and 3), similarly to the findings of Cereda et al. (4) in patients with
ALI/ARDS ventilated with comparable levels of PEEP (about 11 cmH2O, on average).
Brochard et al. in patients (3) and Lu et al. in sheep (5) found a smaller decrease in lung
volume when endotracheal suctioning was performed with disconnection from the ventilator
(about 400 ml), partly because low levels of PEEP (5 cmH2O) or no PEEP was used. The
large volume fall observed after disconnection, may suggest that PEEP could have produced

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some degree of alveolar overdistension (17). As well, disconnection may have allowed the
exhalation of gas, which was previously trapped in the lung as a result of dynamic
hyperinflation (18-20). The fall in lung volume during endotracheal suctioning after ventilator
circuit disconnection results both from the loss of the positive airway pressure generated by
mechanical ventilation with PEEP, and from the negative pressure applied during suctioning
(3, 5) (Figure 1). Interestingly, the lung volume fall due to the application of the negative
pressure alone, after disconnection, was identical to the drop in lung volume observed when
suctioning was performed without disconnection, suggesting that avoiding disconnection from
the ventilator allows to prevent approximately 50% of the lung volume fall observed during
suctioning after disconnection.
Performing endotracheal suctioning without disconnection from the ventilator,
through the swivel adapter of the catheter mount and with a closed system, limited the lung
volume fall but not to a full extent (Figures 1 and 3). This confirms that both the loss of the
positive airway pressure due to disconnection and the application of a negative pressure are
involved in the occurrence of the alveolar collapse associated with endotracheal suctioning.
This suggests that the use of a closed suctioning system could be recommended in patients
ventilated with high PEEP levels, who are at greater risk of large lung volume fall during
suctioning with conventional techniques.
The use of in-line suction catheters has been found effective in limiting or preventing
endotracheal suctioning-induced hypoxemia and lung volume fall (4, 21, 22). We observed a
decrease in end-expiratory lung volume with the closed-suction system, which was larger than
previously reported by Cereda et al. in similar patients (4). In the latter study, however, the
trigger sensitivity was set at 2 cmH2O and the ventilator was thus allowed to autocycle
during suctioning with the closed system, while this phenomenon did not occur in our study.
Ventilator autocycling during endotracheal suctioning could be efficient to compensate for

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some volume lost during suctioning and contribute to further prevent the lung volume drop
with the closed system, explaining the differences with the present study. This hypothesis is
confirmed by the fact that SpO2 did not change during suctioning with the closed-suction
system in the study by Cereda et al., while we found a small SpO2 decrease (Figure 6). Our
results showed the pure effect of the closed system use on lung volume during endotracheal
suctioning, while the findings of Cereda et al. resulted by the combined effects of the closedsuction system and specific ventilatory settings. In fact, the effect of a closed-suction system
on lung volume during suctioning may depend upon the ventilatory mode and settings, the
suctioning technique and duration, as well as the ratio between the diameters of the suction
catheter and the endotracheal tube (23-25).

Endotracheal suctioning-induced changes in alveolar recruitment

Changes in end-expiratory lung volume were measured together with true alveolar
recruitment. Although mathematically coupled, changes in end-expiratory lung volume and
recruitment are not equivalent (26). End-expiratory lung volume refers to PEEP-induced net
increase in lung volume above the elastic equilibrium volume of the respiratory system at
ZEEP. Alveolar recruitment is the amount of lung volume exceeding the volume increase
predicted by the pressure-volume relationship at ZEEP (27). Indeed, alveolar recruitment
expressed at 20 cmH2O, for instance, will vary with the amount of collapsed lung units which
can be reopened by the prolonged application of a continuous positive airway pressure. One
could imagine a situation where the lung volume loss is regained at the expense of a few
alveoli kept open and hyperinflated, while the more unstable alveoli cannot be reopened and
remain closed. Therefore, in patients with large lung areas remaining open and normally
aerated at ZEEP, endotracheal suctioning-induced changes in end-expiratory lung volume and
alveolar recruitment might be quite different.

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Several findings of the present study are consistent with the fact that the major
abnormality encountered with endotracheal suctioning is the fall in lung volume (Figure 5),
including the changes in compliance (3). These changes correlated with the changes in
alveolar recruitment and with the drop in SpO2. The larger the endotracheal suctioninginduced fall in lung volume, the lower the short-term efficacy of PEEP to recruit collapsed
alveoli after suctioning, and the larger the decrease in SpO2. Indeed, the effect of PEEP on
alveolar recruitment is a time-dependent phenomenon and depends upon how much of the
lungs have been recruited during the previous ventilation, as recently reported (28).

Effect of endotracheal suctioning on oxygen saturation

We found that suctioning with the closed system and through the swivel adapter of the
catheter mount were equally effective in limiting the large oxygen desaturation observed
when endotracheal suctioning was performed disconnecting the patient from the ventilator
(Figure 6). Although SpO2 can sometimes poorly reflect the variations in arterial partial
pressure of oxygen (29), it is largely used in the clinical setting to monitor mechanically
ventilated patients (30). The correlations found between SpO2, alveolar recruitment and endexpiratory lung volume, although weak, tend to reinforce a causal relationship. Other
mechanisms could explain the SpO2 drop observed even when lung volume was maintained.
Suctioning could have induced hemodynamic changes, which, by modifying the
ventilation/perfusion ratio, could explain the transient impairment in SpO2 even when lung
volume was preserved. Another explanation could be that endotracheal suctioning-induced
bronchoconstriction may result in an increase in venous admixture (5). We observed only a
small increase in total respiratory system resistances after suctioning performed with
disconnection, through the swivel adapter and with the closed system, whereas it did not
change after the two techniques performed while triggering pressure-supported breaths. The

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small magnitude of these changes in the context of a decrease in lung volume makes difficult
to ascertain if this corresponded to a true bronchoconstriction or to the effects of lung volume
changes on respiratory system resistances. The increase in lung volume and alveolar
recruitment observed when a recruitment maneuver was performed during suctioning
counterbalanced the increase in total respiratory system resistances observed with the other
techniques.

Effect of endotracheal suctioning on the respiratory pressure-volume curve

Endotracheal suctioning-induced changes in alveolar recruitment were strongly
correlated with changes in linear compliance at ZEEP (Figure 7). In a recent study we found
that linear compliance above the lower inflection point may reflect the amount of lung areas
recruitable with PEEP (15). The tight relationship between suctioning-induced changes in
alveolar recruitment and in linear compliance we found in the present study supports this idea.
However, derecruitment caused by suctioning with ventilator disconnection was accompanied
by a decrease in linear compliance. We have previously shown that derecruitment induced by
decremental PEEP levels produced a progressive increase in linear compliance (15). In other
terms, the more recruitable the lung during the pressure-volume curve maneuver at ZEEP, the
higher the linear compliance. When PEEP is applied and the lung is recruited, there are less
recruitable lung areas and the linear compliance is lower. In the present study, the duration of
suctioning maneuvers and the amount of lung collapse could explain the lower linear
compliance observed after suctioning. In our previous study, the pressure-volume curve from
ZEEP was recorded after a single 6-sec expiration to the elastic equilibrium volume at ZEEP.
The lung areas, which collapsed during this expiration, were completely reopened during the
following large low-flow insufflation performed to record the pressure-volume curve. In this
context, a high linear compliance at ZEEP indicated that the collapsed lung areas were

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recruited during the large insufflation and could be kept open with PEEP. In the present study,
the duration of the suctioning procedure (30 seconds) and the large lung volume loss during
suctioning could make the collapsed lung areas much more difficult to recruit during
subsequent pressure-volume curve maneuver. Therefore, the lower compliance at ZEEP may
indicate that the lung zones collapsed during suctioning cannot be fully reopened during the
following pressure-volume curve. The lung volume fall during suctioning, below the
functional residual capacity, profoundly modified the pressure-volume relationship of the
respiratory system and may explain the bidirectional findings regarding linear compliance.

Prevention of endotracheal suctioning-related adverse events

It has been shown that repetitive alveolar collapse and reopening can be injurious for
the lung (6, 7, 31-33). Mead and coworkers showed, in a model of heterogeneous lung, that
atelectatic regions can be exposed to shear stress generated by the recruitment of collapsed
alveoli and the overdistension of the alveolar units adjacent to atelectatic zones (31). The
application of a negative pressure could further increase shear forces resulting in lung damage
(2). Lung injury resulting from repetitive alveolar opening and closing can affect the release
of inflammatory mediators into the lung and the systemic circulation (7, 33). Therefore,
preventing the periodic alveolar derecruitment induced by endotracheal suctioning could be
more clinically relevant than its reversal in patients with ALI/ARDS.
In the present study, using the triggering function of the ventilator during endotracheal
suctioning to deliver 40 cmH2O pressure-supported breaths seemingly induced a sort of
recruitment maneuver during suctioning. This maneuver fully prevented the suctioninginduced derecruitment and can be incorporated in a global strategy to avoid derecruitment and
hypoxemia in the most severe ALI/ARDS patients (34). A previous study proposed the use of
a special, modified endotracheal tube as a method to prevent lung volume fall during

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suctioning (3). However, the clinical application of that method was greatly limited by the use
of special equipment. The present study describes a simplest way to fully prevent, not simply
reverse, endotracheal suctioning-related derecruitment.

Study limitations
The present study did not address the efficacy of the different suctioning techniques in
terms of quantity of secretions removed. However, the wall pressure, the catheter size, the
duration of suctioning and the technique for introducing and withdrawing the catheter, all
influencing the efficacy of endotracheal suctioning, were kept strictly similar during the
study. To our knowledge, no study has clearly shown a greater efficacy of a specific
suctioning procedure compared to others. Concern has been expressed about the efficacy of
the closed system in removing secretions. Few data exist on this issue, with anecdotal reports
suggesting a lower efficacy of the closed system compared to the conventional, open
technique (35). Nevertheless, in a study specifically addressing this issue, no significant
difference between the amount of secretions removed with the closed-circuit catheter and with
a conventional catheter was found (36). Increasing the degree of applied negative pressure can
increase the efficiency of suctioning, but also augments the risk for mucosal trauma (37).
Because patients were sedated and paralyzed, the effect of the studied suctioning
techniques in spontaneously breathing patients was not assessed. Avoiding paralysis might
partly prevent the lung volume fall during endotracheal suctioning, by allowing patients to
cough for instance. On the other hand, introducing the suction catheter into the airways
without interrupting mechanical ventilation may impede the ventilator to efficiently assist the
patient during suctioning, causing a major patient-ventilator dissynchrony and patient
discomfort (24). Therefore, the interference of the suction catheter with mechanical

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ventilation in spontaneously breathing patients, as well as the effect of specific ventilatory
modes and settings needs further studies.
In summary, we have found that, in ALI/ARDS patients, avoiding disconnection from
the ventilator and, more efficiently, using a closed-suction system allowed to minimize the
adverse effects of endotracheal suctioning on lung volume, alveolar recruitment and
oxygenation. A recruitment maneuver, performed by triggering pressure-supported breaths
during suctioning, fully prevented the lung volume fall and mechanical derangements of
respiratory system, allowing to increase alveolar recruitment.

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N, Lemaire F, Harf A. Constant-flow insufflation prevents arterial oxygen desaturation during
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the respiratory system predicts effects of PEEP in ARDS: "Occlusion" versus "Constant flow"
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Comparison with the lower inflection point, oxygenation, and compliance. Am J Respir Crit
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23. Baier H, Begin R, Sackner MA. Effect of airway diameter, suction catheters, and the
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26. Malbouisson LM, Muller JC, Constantin JM, Lu Q, Puybasset L, Rouby JJ. Computed
tomography assessment of positive end-expiratory pressure-induced alveolar recruitment in
patients with acute respiratory distress syndrome. Am J Respir Crit Care Med 2001;163:14441450.
27. Katz JA, Ozanne GM, Zinn SE, Fairley HB. Time course and mechanisms of lung-volume
increase with PEEP in acute pulmonary failure. Anesthesiology 1981;54:9-16.
28. Crotti S, Mascheroni D, Caironi P, Pelosi P, Ronzoni G, Mondino M, Marini JJ, Gattinoni
L. Recruitment and derecruitment during acute respiratory failure . A clinical study. Am J
Respir Crit Care Med 2001;164:131-140.
29. Van de Louw A, Cracco C, Cerf C, Harf A, Duvaldestin P, Lemaire F, Brochard L.
Accuracy of pulse oximetry in the intensive care unit. Intensive Care Med 2001;27:16061613.
30. Jubran A. Pulse oximetry. In: Tobin MJ, editor. Principles and practice of intensive care
monitoring. New York: McGraw Hill; 1998, p. 261-288.
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32. Muscedere JG, Mullen JBM, Gari K, Bryan AC, Slutsky AS. Tidal ventilation at low
airway pressures can augment lung injury. Am J Respir Crit Care Med 1994;149:1327-1334.
33. Chiumello D, Pristine G, Slutsky AS. Mechanical ventilation affects local and systemic
cytokines in an animal model of acute respiratory distress syndrome. Am J Respir Crit Care
Med 1999;160:109-116.
34. NIH ARDS Trials Network. Prospective, randomized, multi-center trial of higher endexpiratory lung volume/lower FiO2 versus lower end-expiratory lung volume/higher FiO2
ventilation in acute lung injury and acute respiratory distress syndrome. Assessment of low
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protocol available at http://hedwig.mgh.harvard.edu/ardsnet/.
35. Noll ML, Hix CD, Scott G. Closed tracheal suction systems: effectiveness and nursing
implications. AACN Clin Issues Crit Care Nurs 1990;1:318-328.
36. Witmer MT, Hess D, Simmons M. An evaluation of the effectiveness of secretion removal
with the Ballard closed-circuit suction catheter. Respir Care 1991;36:844-848.
37. Kuzenski BM. Effect of negative pressure on tracheobronchial trauma. Nurs Res
1978;27:260-263.

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FIGURE LEGENDS

Figure 1
Tracings of airway pressure and volume, measured by thoracic respiratory inductive
plethysmography, during endotracheal suctioning procedures in a representative patient (#3).
Changes in end-expiratory lung volume (EELV tot) were measured as the difference
between the value of end-expiratory lung volume of the cycle immediately preceding the
suctioning procedure and the minimum value recorded during suctioning. When suctioning
was performed after disconnecting patient from the ventilator, a first drop in lung volume was
observed after disconnection (DISCONNECTION) followed by a second drop (NEGATIVE
PRESSURE) when negative pressure was applied. In this patient, disconnection from the
ventilator contributed more than negative pressure to the total lung volume fall recorded
during the entire suctioning procedure. Positive end-expiratory pressure was totally lost
during DISCONNECTION, partially maintained during SWIVEL and CLOSED, and fully
preserved when pressure-supported breaths were triggered during suctioning. Note the
pressure drop at the beginning of the suctioning maneuver with SWIVEL, related to the
opening of the swivel adapter of the catheter mount before introducing the suction catheter.
This pressure drop was avoided with the closed system. When suctioning was performed after
switching from volume-control to pressure support ventilation, trigger sensitivity was set at
1 cmH2O and pressure support was set in order to have a peak inspiratory pressure of 40
cmH2O. In such a way, as suctioning was performed intermittently, pressure-supported
breaths were triggered only when the negative pressure was applied.
DISCONNECTION: endotracheal suctioning performed after the disconnection from the
ventilator; SWIVEL: endotracheal suctioning performed through the swivel adapter of the
catheter mount; CLOSED: endotracheal suctioning performed with the closed system;

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SWIVELPSV: endotracheal suctioning performed through the swivel adapter of the catheter
mount, while triggering pressure-supported breaths during suctioning; CLOSEDPSV:
endotracheal suctioning performed with the closed system, while triggering pressuresupported breaths during suctioning.

Figure 2
Flow-chart of the protocol and measurements with the studied suctioning techniques. Elastic
pressure-volume curves from positive end-expiratory pressure and from zero end-expiratory
pressure were acquired five minutes before endotracheal suctioning and forty-five seconds to
one minute after suctioning. End-expiratory lung volume was measured just before
suctioning, at the end of endotracheal suctioning, one breath after suctioning and forty-five
seconds to one minute after suctioning, just before pressure-volume curves recording. Arterial
oxygen saturation was continuously recorded before, during and after endotracheal suctioning
up to pressure-volume curves recording. Each suctioning procedure (insertion of the suction
catheter, intermittent suctioning and catheter removal) lasted 25 to 30-s.
PEEP: positive end-expiratory pressure; ZEEP: zero end-expiratory pressure; Pel-V curves:
elastic pressure-volume curves; SpO2: pulse oximeter oxygen saturation; EELV: endexpiratory lung volume.

Figure 3
Changes in end-expiratory lung volume during endotracheal suctioning, one breath and one
minute after suctioning with the studied techniques. A very large drop in end-expiratory lung
volume was observed with DISCONNECTION. The fall in lung volume was limited with
SWIVEL and CLOSED (P<0.01) and it was almost avoided when a recruitment maneuver
(switch to pressure support ventilation with a total peak inspiratory pressure set at 40 cmH2O)

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was performed during suctioning (P<0.01). One minute after suctioning, lung volume was
still not restored with DISCONNECTION (P<0.01), it was almost totally recovered with both
SWIVEL and CLOSED (P<0.01 compared to DISCONNECTION, P=NS between SWIVEL
and CLOSED) and it increased with both SWIVELPSV and CLOSEDPSV (P<0.01). SD was
omitted for clarity.
EELV: changes in end-expiratory lung volume; DISCONNECTION: endotracheal
suctioning performed after the disconnection from the ventilator; SWIVEL: endotracheal
suctioning performed through the swivel adapter of the catheter mount; CLOSED:
endotracheal suctioning performed with the closed system; SWIVELPSV: endotracheal
suctioning performed through the swivel adapter of the catheter mount, while triggering 40
cmH2O pressure-supported breaths during suctioning; CLOSEDPSV: endotracheal suctioning
performed with the closed system, while triggering 40 cmH2O pressure-supported breaths
during suctioning.

Figure 4
Pressure-volume curves obtained from zero end-expiratory pressure (ZEEP) and from positive
end-expiratory pressure (PEEP), before (left panels) and after (right panels) endotracheal
suctioning with the studied techniques, in a representative patients (#4). PEEP-induced
recruited volume was measured at the elastic pressure of 20 cmH2O and is indicated by the
line between ZEEP and PEEP curves. Recruitment decreased after suctioning with
disconnection and through the swivel adapter, it did not change with the closed system, and
increased when pressure-supported breaths were triggered during suctioning. A =
endotracheal suctioning after disconnection from the ventilator; B = suctioning without
disconnection from the ventilator, introducing the suction catheter through the swivel adapter
of the catheter mount; C = endotracheal suctioning with a closed system; D = endotracheal

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suctioning through the swivel adapter, while triggering pressure-supported breaths during
suctioning; E = endotracheal suctioning with a closed system, while triggering pressuresupported breaths during suctioning.

Figure 5
Values of PEEP-induced alveolar recruitment measured before (open bars) and after (black
bars) endotracheal suctioning with the studied techniques. After suctioning, recruitment was
significantly smaller with DISCONNECTION and SWIVEL. It did not change with
CLOSED, while it increased significantly with both SWIVELPSV and CLOSEDPSV.
Vrecr: alveolar recruitment; DISCONNECTION: endotracheal suctioning performed after the
disconnection from the ventilator; SWIVEL: endotracheal suctioning performed through the
swivel adapter of the catheter mount; CLOSED: endotracheal suctioning performed with the
closed system; SWIVELPSV: endotracheal suctioning performed through the swivel adapter of
the catheter mount, while triggering 40 cmH2O pressure-supported breaths during suctioning;
CLOSEDPSV: endotracheal suctioning performed with the closed system, while triggering 40
cmH2O pressure-supported breaths during suctioning.
* P<0.01, compared to before endotracheal suctioning.

Figure 6
Correlation between changes in alveolar recruitment and in end-expiratory lung volume one
minute after endotracheal suctioning with the studied suctioning techniques.
EELV: changes in end expiratory lung volume; Vrecr: alveolar recruitment.

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Figure 7
Individual and mean values of the drop in arterial oxygen saturation observed during
endotracheal suctioning with the studied techniques. Data were not available for patient #2.
The changes in arterial oxygen saturation with SWIVEL, CLOSED, SWIVELPSV and
CLOSEDPSV were significantly smaller than with DISCONNECTION.
SpO2: changes in pulse oximeter oxygen saturation; DISCONNECTION: endotracheal
suctioning performed after the disconnection from the ventilator; SWIVEL: endotracheal
suctioning performed through the swivel adapter of the catheter mount; CLOSED:
endotracheal suctioning performed with the closed system; SWIVELPSV: endotracheal
suctioning performed through the swivel adapter of the catheter mount, while triggering 40
cmH2O pressure-supported breaths during suctioning; CLOSEDPSV: endotracheal suctioning
performed with the closed system, while triggering 40 cmH2O pressure-supported breaths
during suctioning.

Figure 8
Correlation between changes in linear compliance of the elastic pressure-volume curve
recorded from zero end-expiratory pressure and in alveolar recruitment with the studied
suctioning techniques.
CLIN at ZEEP: changes in linear compliance of the pressure-volume curve from zero endexpiratory pressure; Vrecr: changes in alveolar recruitment.

28

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TABLE 1
General characteristics of the patients.
Days of
Patient Age
No.

(y)

32

Cause of

Underlying

ALI/ARDS

disease

Acute

Nephrotic

pancreatitis

syndrome

PaO2/FiO2 PEEPEXT
(mmHg)

mechanical

PEEPi

(cmH2O) (cmH2O)

FiO2

LIS

ventilation

Days of
ALI/ARDS Outcome

93

10

2.1

3.25

22

Died

Aortic stenosis

180

10

4.5

2.5

Survived

Alveolar
2

77
hemorrhage

57

Pneumonia

Diabetes

75

13

2.6

Survived

76

Pneumonia

Aortic stenosis

226

12

2.5

0.5

2.5

Survived

38

Viral hepatitis

190

10

1.9

0.5

2.75

Survived

Aortic aneurysm

176

16

3.1

0.5

Survived

100

14

1.8

0.6

3.5

11

Died

Subarachnoid
hemorrhage
Massive blood
6

55
transfusion

Acute lymphoid
7

35

Sepsis
leukemia

46

Pneumonia

Alcoholism

92

12

4.6

3.5

Died

57

Pneumonia

Renal cancer

157

12

3.4

0.7

2.75

Survived

Mean

53

143

12

0.75

2.97

SD

17

54

0.24

0.38

Definition of abbreviations: ALI: acute lung injury; ARDS: acute respiratory distress
syndrome; PEEPEXT: external positive end-expiratory pressure; PEEPi: intrinsic positive endexpiratory pressure; LIS: lung injury score.

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TABLE 2
Individual values of change in end-expiratory lung volume during and just after endotracheal
suctioning, with the studied suctioning technique.
EELV during suctioning (ml)

EELV just after suctioning (one breath) (ml)

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

-1416

-666

-502

-213

-213

-1114

-115

-96

42

-154

-884

-276

-222

-106

-46

-578

-40

-80

142

100

-1962

-1155

-833

-115

-157

-1280

-95

-169

31

-1452

-839

-705

-471

-841

-1067

-260

73

-301

-571

-466

-295

15

-141

-556

-230

-83

153

-76

-1846

-1195

-553

-442

-789

-1325

-491

-299

-79

-130

-843

-394

-693

-112

-9

-671

-168

-190

-11

19

-2092

-1307

-253

-26

-31

-1921

-1017

-102

51

65

-2124

-301

-726

-47

-325

-1530

-70

-155

65

-5

Mean

-1466

-733 *

-531 *

-168 *

-284 * ll

-1116

-276 *

-122 *

7*

-16 *

SD

586

406

228

176

317

460

310

101

136

86

Definitions

of

abbreviations:

EELV:

change

in

end-expiratory

lung

volume;

DISCONNECTION: endotracheal suctioning performed after the disconnection from the

ventilator; SWIVEL: endotracheal suctioning performed through the swivel adapter of the
catheter mount; CLOSED: endotracheal suctioning with the closed system; SWIVELPSV:
endotracheal suctioning performed through the swivel adapter of the catheter mount, while
triggering pressure-supported breaths during suctioning; CLOSEDPSV: endotracheal
suctioning performed with the closed system, while triggering pressure-supported breaths
during suctioning.
* P<0.01, compared to DISCONNECTION; P<0.01, compared to SWIVEL; P<0.05,
compared to SWIVEL; P<0.01, compared to CLOSED; P<0.05, compared to CLOSED; ll
P=0.05, compared to CLOSED.

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TABLE 3
Changes in pressure-volume curve from zero end-expiratory pressure and respiratory
mechanics with the different endotracheal suctioning techniques.
DISCONNECTION

SWIVEL

CLOSED

SWIVELPSV

CLOSEDPSV

Before

After

Before

After

Before

After

Before

After

Before

After

13.5 3

12.5 2.4

12.9 3.3

13.1 3.2

14.6 2.8

14.1 1.7

13.1 3.1

16 2.7 *

14.1 3.6

16 3

VLIP, ml

241 171

152 83

208 126

201 131

280 202

209 146

196 111

356 210 *

257 173

297 173

C1, ml/cmH2O

28.1 15.9

21 7.1 *

25.7 11.2

26.6 11.3

28.9 18.1

23.8 15.8

24.9 8.8 36.3 23.8 * 26.7 14.2

28.6 16

CLIN, ml/cmH2O

71.1 23.1 65.5 20.7 70.6 19.1 65.9 18.1 68.3 19.3

68 19.6

67.9 20.8 75.5 22.7 67.6 20.4

72.8 22

PPEAK, cmH2O

32.8 3.8

34 4.5

32.9 4

34.2 5.4

32.8 3.7

32.3 3.2

33 3.7

31 3.4

32.7 3.8

30.7 3.8

PPLAT, cmH2O

26.6 4

26.9 3.6

26.7 3.9

26.6 4.8

26.7 3.6

25.9 3 *

26.8 4

25.2 3.8 *

27 3.9

25.1 3.9

11.9 3.5 *

10.3 1.6

12.6 3 *

9.8 2.2

10.5 2.3

10.3 1.2

9.6 2.1

9.2 2

9.2 2.1

PLIP, cmH2O

RRS, cmH2OL-1s-1 10.2 1.4

Definitions of abbreviations: PLIP: pressure at the lower inflection point of the pressurevolume curve from zero end-expiratory pressure; VLIP: volume at the lower inflection point of
the pressure-volume curve from zero end-expiratory pressure; C1: compliance of the first part
of the pressure-volume curve from zero end-expiratory pressure, below the lower inflection
point; CLIN: compliance of the linear segment of the pressure-volume curve from zero endexpiratory pressure, above the lower inflection point; PPEAK: peak airway pressure; PPLAT:
end-inspiratory plateau pressure; RRS: total respiratory resistance; DISCONNECTION:
endotracheal suctioning performed after the disconnection from the ventilator; SWIVEL:
endotracheal suctioning performed through the swivel adapter of the catheter mount;
CLOSED: endotracheal suctioning performed with the closed system; SWIVELPSV:
endotracheal suctioning performed through the swivel adapter of the catheter mount, while
triggering pressure-supported breaths during suctioning; CLOSEDPSV: endotracheal
suctioning performed with the closed system, while triggering pressure-supported breaths
during suctioning.
* P<0.05, compared to before suctioning; P<0.01, compared to before suctioning.

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Figure 1
DISCONNECTION
Airway Pressure (cmH2O)

40

30

20

10

10

1500

1000

1000

500

500

0
-500

DISCONNECTION

NEGATIVE
PRESSURE

30

20

10

-1500

30

20

10

1500

1500

1000

1000

500

500

Volume (ml)

-500

EELV tot

-1000

SWIVELPSV

40

ES

50

Airway Pressure (cmH2O)

40

EELV tot

-1000

-2500

CLOSED

50

0
-500

-2000

ES

-2500

Airway Pressure (cmH2O)

20

1500

-2000

Volume (ml)

30

-1500

0
-500

* EELV tot

-1000
-1500

-1500

-2000

-2000

ES

-2500

-2500

ES

CLOSEDPSV

50

Airway Pressure (cmH2O)

40

EELV tot
-1000

SWIVEL

50

Volume (ml)

Volume (ml)

Airway Pressure (cmH2O)

50

40

30

20

10

1500
1000

Volume (ml)

500
0
-500

* EELV tot

-1000
-1500
-2000
-2500

ES

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Figure 2

5-min

SpO 2
EELV

SpO 2
EELV

SpO 2
EELV

Just before
suctioning

1 breath after
suctioning

Just before
Pel-V curves

Suctioning
(25 to 30-s)

45-s to 1- min

End of suctioning

PEEP and ZEEP

P el-V curves

SpO 2
EELV

PEEP and ZEEP

Pel-V curves

33

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Figure 3

Before suctioning

Suctioning

After suctioning
(one breath)

After suctioning
(45-s to 1-min)

200
0

EELV (ml)

-200
-400

DISCONNECTION
-600

SWIVEL
-800

CLOSED
-1000

CLOSEDPSV

-1200

SWIVELPSV

-1400
-1600
p < 0.001

p < 0.001

p < 0.001

34

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Figure 4

Volume (ml)

Before suctioning
1400

1400

1050

1050

700

700

350

350

Volume (ml)

10

20

30

40

50

1400

1400

1050

1050

700

700

350

350

Volume (ml)

10

20

30

40

50

1400

1400

1050

1050

700

700

350

350

Volume (ml)

10

20

30

40

50

1400

1400

1050

1050

700

700

350

350

Volume (ml)

20

30

40

50

10

20

30

40

50

10

20

30

40

50

10

20

30

40

50

10

20

30

40

50

0
0

10

0
0

0
0

After suctioning

10

20

30

40

50

1400

1400

1050

1050

700

700

350

350

0
0

10

20

30

40

50

Elastic Pressure (cm H2O)

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Figure 5

Before suctioning
After suctioning
500

Vrecr (ml)

400

300

200

100

0
DISCONNECTION

SWIVEL

CLOSED

SWIVELPSV

CLOSEDPSV

36

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Figure 6

200
Y = 6.9 + 0.28 X,

150

rho = 0.88, p < 0.001

Vrecr (ml)

100
50
DISCONNECTION

0
SWIVEL

-50

CLOSED

-100

CLOSEDPSV

-150

SWIVELPSV

-200
-900

-450

450

900

EELV 1-min after suctioning (ml)

37

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Figure 7

DISCONNECTION SWIVEL

CLOSED

SWIVELPSV

CLOSEDPSV

-5

SpO2 (%)

Pt #1
Pt #3

-10

Pt #4
p < 0.05

-15

p < 0.05

p < 0.05

p < 0.05

Pt #5
Pt #6
Pt #7
Pt #8

-20

Pt #9
mean

-25

38

R1
Figure 8

30
Y = 1.1 + 0.2 X,

CLIN at ZEEP (%)

20

rho = 0.9, p < 0.001

10
DISCONNECTION
0

SWIVEL
CLOSED

-10

CLOSEDPSV
-20

-30
-150

SWIVELPSV

-100

-50

50

100

150

Vrecr (%)

39

ONLINE-DATA SUPPLEMENT

Prevention of Endotracheal Suctioning-induced Alveolar Derecruitment in Acute Lung

Injury

Salvatore M. MAGGIORE1, Franois LELLOUCHE2, Jrme PIGEOT2, Solenne TAILLE2,

Nicolas DEYE2, Xavier DURRMEYER2, Jean-Christophe RICHARD3, Jordi MANCEBO4,
Franois LEMAIRE2, Laurent BROCHARD2
1

Department of Anesthesiology and Intensive Care, Agostino Gemelli Teaching Hospital,

Universit Cattolica del Sacro Cuore, Rome, Italy;

Medical Intensive Care Unit, INSERM

U492, Henri Mondor Teaching Hospital, AP-HP, Paris XII University, Crteil, France;

Medical Intensive Care Unit, Charles Nicolle Teaching Hospital, Rouen, France; 4 Servei de
Medicina Intensiva, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain

Send all correspondence including reprint requests to:

Prof. L. Brochard, Ranimation Mdicale, Hpital Henri Mondor, 94000 Crteil, France.
Phone: +33 1 49 81 23 92; Fax: +33 1 42 07 99 43;
E-mail: [email protected]

This study was supported by INSERM U492. The equipment was kindly furnished by TYCO
Healthcare, CA, USA.

Running Title: Endotracheal Suctioning in Acute Lung Injury

Descriptor numbers: 2 - 10 -13
Word count (text without references): 1625

R1

METHODS

Measurement of end-expiratory lung volume

Changes in end-expiratory lung volume (EELV) were measured by respiratory
inductive plethysmography (RIP) (AMI Model 150; Ambulatory Monitoring Inc., NY, USA)
operating in the DC mode. This is a differential linear transformer, composed of a sensor
mounted on a flexible but non-extensible belt and positioned around the patient at the nipple
level, as previously described (E1-E3). Because in the DC-coupled mode the oscillator drift is
sensitive to temperature (E4), we waited for 60 minutes before taking any measurements to
allow for thermal equilibrium. In paralyzed subjects, the respiratory system can be considered
a system with a single degree of freedom, without variation of thoraco-abdominal partitioning
of volume (E1). Therefore, since all patients were paralyzed, changes in lung volume were
computed from a single signal, the rib cage displacement. To verify the validity of this
assumption, the double-coil, thoracic and abdominal, RIP was used in five paralyzed patients.
The RIP deflections for the thoracic and the abdominal coils were highly correlated (R2
0.97) with and directly proportional to the volume measured by integrating the signal obtained
from a heated calibrated Fleisch No. 1 pneumotachygraph (Lausanne, Switzerland), connected
to a differential pressure transducer (Validyne MP45 2.5 cmH2O; Northridge, CA, USA)
and inserted between the endotracheal tube and the ventilator circuit. Signals were digitized at
200 Hz and sampled using an analogic/digital system (MP100; Biopac systems, Santa
Barbara, CA). The calibration procedure was conducted during mechanical ventilation by
comparing EELV measured by thoracic RIP with the integrated flow signal obtained from
the pneumotachygraph. Calibration lines were calculated by linear regression and all
coefficients of linear regression (R2) were 0.96. Mean Y-intercept was 0.02 0.14 mV and
not different from zero (P=NS). EELV was calculated as the difference between the volume

R1

measured at the end of expiration just before suctioning and the volume measured at the end
of suctioning. EELV was also measured at the end of expiration of the first breath following
endotracheal suctioning, back in volume-controlled mode, and one minute after suctioning,
before elastic pressure-volume (Pel-V) curves recording. Because the drift of the RIP signal
could affect measurement of lung volume, we recorded in each patient the signal of the RIP
thoracic coil over 5 minutes before each suctioning maneuver, without interfering with the
basal ventilation and after calibrating the instrument. This time interval was considered
sufficient for the drift assessment because the signal recording performed to assess lung
volume changes during and after suctioning lasted approximately 90 seconds (30 seconds
during suctioning and 60 seconds after suctioning). The 5-min baseline drift of RIP averaged
0.5 6.9 ml and changed over a narrow range in single patients (min -8.5 8.3 ml, max 13.4
22.5 ml) and between the different suctioning techniques (min -5.4 10.6 ml, max 6.1
23.1 ml) (P=NS).
When suctioning was performed after disconnection from the ventilator, the
contribution of disconnection from the ventilator alone and of negative pressure to the total
lung volume drop was quantified. Looking at the RIP tracings recorded during suctioning
performed after disconnection, it was possible to identify a first drop in lung volume
immediately after disconnection, followed by a second drop when the negative pressure was
applied. The first drop was the EELV due to disconnection alone, while the second drop was
the additional EELV induced by applying the negative pressure. Their sum was the EELV
due to the whole suctioning procedure.

Measurement and analysis of elastic pressurevolume curves

The system including a computer controlled Servo Ventilator 900C (Siemens-Elema
AB, Solna, Sweden) and the technique for acquiring Pel-V curves, based on the low flow

R1

insufflation method, have been previously described in detail (E5-E7). Volumes were
measured as BTPS. The signals were fed into the computer and A/D converted at 50 Hz.
Application of analog signals to the external control socket of the ventilator permitted the
computer to control ventilatory rate, level of positive end-expiratory pressure (PEEP), and
minute volume. The external control signal had an immediate effect. If the external signal for
minute ventilation was oscillating during a specific inspiration, this led to a modulated
oscillating inspiratory flow. This allowed Pel-V curves to be obtained either from PEEP or
from zero end-expiratory pressure (ZEEP). After an expiration prolonged to 8 s, during which
the pressure was either maintained at PEEP or decreased to ZEEP, a high volume was
insufflated during a 6-s-long inspiratory phase. This volume was set in order to maintain endinspiratory pressure below 50 cmH2O. If the pressure reached 50 cmH2O before the volume
was entirely delivered, the insufflation was automatically stopped. During insufflation, the
flow was sinusoidally modulated at 1 Hz. This variation in flow rate made it possible to
calculate inspiratory resistances of the respiratory system for further subtraction from the
pressure signal, thus allowing the elastic pressure of the respiratory system to be computed.
The following expiration was prolonged in order to allow complete expiration of the high
insufflated volume.
The recorded data for flow and pressure from the insufflation period were analyzed in
order to construct the Pel-V curve. The data were transferred to a spreadsheet (EXCEL 7.0
Microsoft), where the analysis was automatically performed. The different steps required to
determine the elastic pressure from the measured total airway pressure have been recently
described (E5-E7). Total resistive pressure gradient from the Y-piece was calculated from
tube and respiratory system resistances, and Pel was obtained by subtracting resistive pressure
from measured airway pressure.
Each Pel-V curve was mathematically analyzed using a sigmoid model (E5, E8) that

R1

divides each curve into three segments separated by the lower inflection point (LIP) and the
upper inflection point (UIP). The segment before the LIP and the segment after the UIP are
curvilinear and have low compliance values. The steeper segment between LIP and UIP has
higher compliance (CLIN), and is considered linear. LIP and UIP are defined as the points
where the statistical analysis indicates that the Pel-V curve begins to deviate from a straight
line. Accordingly, LIP corresponds to the point where the second derivative of the equation
used for the Pel-V curve mathematical fitting reaches its maximum value. Similarly, UIP
corresponds to the minimum value of the second derivative of the equation.
Pel as a function of volume is described as follows.
Below the LIP:
(1.1)

Pel = PLIP - (VLIP - VMIN)/CLIN ln [(VMIN - VLIP)/(VMIN V)]

Between LIP and UIP:

(1.2)

Pel = PLIP + (V VLIP)/CLIN

Above the UIP:

(1.3)

Pel = PUIP + (VMAX VUIP)/CLIN ln [(VMAX VUIP)/(VMAX V)]

VLIP and PLIP are volume and pressure at LIP, respectively, and VUIP and PUIP are

volume and pressure at UIP, respectively. Below LIP, compliance increases linearly with the
inflated volume from zero (minimal lung volume, VMIN) to VLIP. At the linear segment
between LIP and UIP, the relationship is described by the coefficients VLIP and CLIN. Above
UIP, compliance falls linearly with additional volume, from CLIN to zero at maximum
distension of the lungs, i.e., at VMAX. The coefficients that define the Pel-V curve (i.e., VMIN,
VLIP, CLIN, VUIP, VMAX) are estimated from raw data using a numerical technique involving
determination of the least sum of squared deviations between measured Pel and the equation
describing Pel as a function of volume.
The effective compliance of the first segment of the Pel-V curve recorded from ZEEP

R1

(C1), below LIP, was calculated as: C1 = VLIP / PLIP intrinsic PEEP.

Measurement of alveolar recruitment

PEEP and ZEEP Pel-V curves were plotted on the same volume axis, using PEEPrelated end-expiratory lung-volume change measured during the passive expiration from
PEEP to ZEEP. PEEP-related alveolar recruitment was defined, for a given elastic pressure,
by the volume difference between both curves (E5-E7, E9-E11). This volume represented the
PEEP-induced recruitment of previously collapsed lung units, and was identified by the
upward shift of the PEEP Pel-V curve, relative to the ZEEP Pel-V curve. Alveolar recruitment
was measured at the elastic pressure of 20 cmH2O (E5-E7, E9-E11) (Figure 1).

Measurement of airway pressures and total respiratory resistance

Airway pressure was measured with a differential pressure transducer (MP45,
Validyne, Northridge, CA) connected to the distal end of the endotracheal tube. Peak
inspiratory pressure (PPEAK) and airway pressure 3-5 seconds after the onset of an endinspiratory occlusion (PPLAT) were measured just before and after each suctioning procedure.
Values of airway pressure at end-expiration of a regular breath (PEEPEXT) and 35 seconds
after the onset of an end-expiratory occlusion (PEEPTOT) were measured at the beginning of
the protocol. Intrinsic (PEEPi) was computed as the difference between PEEPTOT and
.

PEEPEXT. Total respiratory resistance (RRS) was calculated as Rtot = (Ppeak - Pplat)/ V ,
.

where V is the inspiratory flow.

Protocol
A 30-min washout period of baseline ventilation was allowed between each suctioning
procedure. For each studied technique, the baseline end-expiratory lung volume was the value

R1

of end-expiratory lung volume of the cycle immediately preceding the suctioning procedures.
When the suctioning maneuver was performed without disconnection from the
ventilator (passing the suction catheter through the swivel adapter of the catheter mount and
using the closed system), while switching to pressure support ventilation, the trigger
sensitivity was set at 1 cmH2O in order to trigger the ventilator while applying the negative
pressure. Therefore, as suctioning was performed intermittently, the fall in airway pressure
triggered pressure-supported breaths only when the negative pressure was applied. In the 30sec duration of the entire suctioning procedure (opening the endotracheal tube, insertion of the
suction catheter, intermittent suctioning, removal of the suction catheter, and closing the
endotracheal tube) an average of 9 pressure-supported breaths were delivered (9.44 1.67 and
9 2.06 breaths with suctioning through the swivel adapter while triggering pressuresupported breaths and with the closed system while triggering pressure-supported breaths,
respectively).

R1

REFERENCES

E1. Dall'ava-Santucci J, Armaganidis A, Brunet F, Dhainaut JF, Chelucci GL, Monsallier JF,
Lockhart A. Causes of error of respiratory pressure-volume curves in paralyzed subjects. J
Appl Physiol 1988;64:42-49.
E2. Brochard L, Mion G, Isabey D, Bertrand C, Messadi AA, Mancebo J, Boussignac G,
Vasile N, Lemaire F, Harf A. Constant-flow insufflation prevents arterial oxygen desaturation
during endotracheal suctioning. Am Rev Respir Dis 1991;144:395-400.
E3. Cereda M, Villa F, Colombo E, Greco G, Nacoti M, Pesenti A. Closed system
endotracheal suctioning maintains lung volume during volume-controlled mechanical
ventilation. Intensive Care Med 2001;27:648-654.
E4. Hudgel DW, Capehart M, Johnson B, Hill P, Robertson D. Accuracy of tidal volume,
lung volume, and flow measurements by inductance vest in COPD patients. J Appl Physiol
1984;56:1659-1665.
E5. Jonson B, Richard J-C, Straus C, Mancebo J, Lemaire F, Brochard L. Pressure-volume
curves and compliance in acute lung injury. Evidence of recruitment above the lower
inflection point. Am J Respir Crit Care Med 1999;159:1172-1178.
E6. Richard J-C, Maggiore SM, Jonson B, Mancebo J, Lemaire F, Brochard L. Influence of
tidal volume on alveolar recruitment. Respective role of PEEP and a recruitment maneuver.
Am J Respir Crit Care Med 2001;163:1609-1613.
E7. Maggiore SM, Jonson B, Richard J-C, Jaber S, Lemaire F, Brochard L. Alveolar
derecruitment at decremental positive end-expiratory pressure levels in acute lung injury.
Comparison with the lower inflection point, oxygenation, and compliance. Am J Respir Crit
Care Med 2001;164:795-801.
E8. Svantesson C, Drefeldt B, Sigurdsson S, Larsson A, Brochard L, Jonson B. A single

R1

computer-controlled mechanical insufflation allows determination of the pressure-volume

relationship of the respiratory system. J Clin Monit Comput 1999;15:9-16.
E9. Ranieri VM, Eissa NT, Corbeil C, Chasse M, Braidy J, Matar N, Milic-Emili J. Effects of
positive end-expiratory pressure on alveolar recruitment and gas exchange in patients with the
adult respiratory distress syndrome. Am Rev Respir Dis 1991;144:544-551.
E10. Ranieri VM, Giuliani R, Fiore T, Dambrosio M, Milic-Emili J. Volume-pressure curve
of the respiratory system predicts effects of PEEP in ARDS: "Occlusion" versus "Constant
flow" technique. Am J Respir Crit Care Med 1994;149:19-27.
E11. Ranieri VM, Mascia L, Fiore T, Bruno F, Brienza A, Giuliani R. Cardiorespiratory
effects of positive end-expiratory pressure during progressive tidal volume reduction
(permissive hypercapnia) in patients with acute respiratory distress syndrome. Anesthesiology
1995;83:710-720.

R1

FIGURE LEGEND

Figure E1
Mean changes in linear compliance of the elastic pressure-volume curve recorded from the
static equilibrium volume at zero end-expiratory pressure with the studied suctioning
techniques. Linear compliance decreased with both DISCONNECTION and SWIVEL
(P<0.01). It did not change after CLOSED (P=NS), and increased with both SWIVELPSV and
CLOSEDPSV (P<0.01).
CLIN at ZEEP: changes in linear compliance of the pressure-volume curve from zero endexpiratory pressure; DISCONNECTION: endotracheal suctioning performed after the
disconnection from the ventilator; SWIVEL: endotracheal suctioning performed through the
swivel adapter of the catheter mount; CLOSED: endotracheal suctioning performed with the
closed system; SWIVELPSV: endotracheal suctioning performed through the swivel adapter of
the catheter mount, while triggering pressure-supported breaths during suctioning;
CLOSEDPSV: endotracheal suctioning performed with the closed system, while triggering
pressure-supported breaths during suctioning.
* P<0.01, compared to DISCONNECTION; P<0.01, compared to SWIVEL; P<0.01,
compared to CLOSED; P<0.05, compared to SWIVELPSV.

R1

TABLE E1
Individual values of pressure at the lower inflection point of the elastic pressure-volume curve
recorded from zero end-expiratory pressure, before and after endotracheal suctioning, with the
studied techniques.
#

PLIP before suctioning (cmH2O)

PLIP after suctioning (cmH2O)

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

14.6

15.6

13.1

14.0

14.0

13.3

14.6

12.6

15.6

15.2

14.9

15.9

15.6

17.5

16.0

15.6

17.5

14.6

16.4

16.6

11.5

8.3

13.3

8.7

11.2

7.8

8.0

12.1

15.3

13.3

14.4

13.2

17.3

13.8

14.5

13.0

13.0

14.0

16.0

19.8

17.1

16.8

18.6

15.2

16.0

12.0

15.7

13.4

19.4

17.9

16.7

15.4

15.4

15.0

13.6

14.7

14.8

16.0

17.5

17.4

10.1

12.1

16.3

13.5

21.0

12.9

9.8

17.2

17.6

18.7

13.9

11.3

12.4

12.9

12.4

10.6

11.0

13.0

17.0

14.6

7.9

7.9

9.5

7.6

7.9

6.9

7.2

8.3

9.6

10.1

Mean

13.5

12.9

14.6

13.1

14.1

12.5

13.1

14.1

16.0*

16.0

SD

3.0

3.3

2.8

3.1

3.6

2.4

3.2

1.7

2.7

3.0

Definitions of abbreviations: PLIP: pressure at the lower inflection point of the pressurevolume curve from zero end-expiratory pressure; DISCONNECTION: endotracheal
suctioning performed after the disconnection from the ventilator; SWIVEL: endotracheal
suctioning performed through the swivel adapter of the catheter mount; CLOSED:
endotracheal suctioning with the closed system; SWIVELPSV: endotracheal suctioning
performed through the swivel adapter of the catheter mount, while triggering pressuresupported breaths during suctioning; CLOSEDPSV: endotracheal suctioning performed with
the closed system, while triggering pressure-supported breaths during suctioning.
* P<0.05, compared to before suctioning.

10

R1

TABLE E2
Individual values of volume at the lower inflection point of the elastic pressure-volume curve
recorded from zero end-expiratory pressure, before and after endotracheal suctioning, with the
studied techniques.
#

VLIP before suctioning (ml)

VLIP after suctioning (ml)

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

139

192

154

93

160

123

191

120

179

195

108

120

144

168

144

112

94

98

150

100

458

206

622

229

470

176

235

531

658

513

190

130

303

170

208

145

178

167

226

332

584

532

612

461

549

315

529

343

696

619

291

200

163

152

116

107

137

169

256

209

130

200

228

246

420

250

148

249

376

326

106

158

63

136

98

85

193

71

480

131

162

130

231

107

148

58

103

135

184

247

Mean

241

208

280

196

257

152

201

209

356*

297

SD

171

126

202

111

173

83

131

146

210

173

Definitions of abbreviations: VLIP: volume at the lower inflection point of the pressurevolume curve from zero end-expiratory pressure; DISCONNECTION: endotracheal
suctioning performed after the disconnection from the ventilator; SWIVEL: endotracheal
suctioning performed through the swivel adapter of the catheter mount; CLOSED:
endotracheal suctioning with the closed system; SWIVELPSV: endotracheal suctioning
performed through the swivel adapter of the catheter mount, while triggering pressuresupported breaths during suctioning; CLOSEDPSV: endotracheal suctioning performed with
the closed system, while triggering pressure-supported breaths during suctioning.
* P<0.05, compared to before suctioning.

11

R1

TABLE E3
Individual values of compliance of the first segment of the elastic pressure-volume curve
recorded from zero end-expiratory pressure, below the lower inflection point, before and after
endotracheal suctioning, with the studied techniques.
#

C1 before suctioning (ml/cmH2O)

C1 after suctioning (ml/cmH2O)

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

DISCONNECTION SWIVEL CLOSED SWIVELPSV CLOSEDPSV

13.2

15.2

14.0

13.2

13.3

12.1

17.5

15.2

15.5

14.8

18.3

16.4

23.6

22.7

20.9

17.8

15.2

15.3

20.3

13.4

61.0

39.6

68.3

40.2

59.4

33.9

40.5

63.2

63.9

63.3

15.3

11.6

22.1

15.3

18.4

14.7

17.8

14.2

17.9

23.2

38.2

35.2

37.3

32.9

37.4

29.7

38.1

28.8

40.5

39.2

33.9

26.0

19.6

20.8

18.7

16.3

20.1

21.1

27.2

24.9

13.4

17.7

14.9

19.9

23.3

21.9

15.6

16.2

22.8

19.3

23.0

41.6

15.4

31.7

19.3

19.7

39.4

13.6

85.8

20.4

36.8

27.8

44.5

27.5

29.5

23.2

35.5

27.0

32.9

38.7

Mean

28.1

25.7

28.9

24.9

26.7

21.0*

26.6

23.8

36.3*

28.6

SD

15.9

11.2

18.1

8.8

14.2

7.1

11.3

15.8

23.8

16.0

Definitions of abbreviations: C1 = compliance of the first segment of the pressure-volume

curve recorded from zero end-expiratory pressure, below the lower inflection point;
DISCONNECTION: endotracheal suctioning performed after the disconnection from the
ventilator; SWIVEL: endotracheal suctioning performed through the swivel adapter of the
catheter mount; CLOSED: endotracheal suctioning with the closed system; SWIVELPSV:
endotracheal suctioning performed through the swivel adapter of the catheter mount, while
triggering pressure-supported breaths during suctioning; CLOSEDPSV: endotracheal
suctioning performed with the closed system, while triggering pressure-supported breaths
during suctioning.
* P<0.05, compared to before suctioning.

12

R1

Figure E1

20
15

CLIN at ZEEP (%)

10
5

0
-5
-10
-15
-20
DISCONNECTION

SWIVEL

CLOSED

SWIVELPSV

CLOSEDPSV

13