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Journal of Critical Care (2012) 27, 37–44

Manual compression of the abdomen to assess expiratory


flow limitation during mechanical ventilation☆
Malcolm Lemyze MD a,⁎, Raphael Favory MD a , Isabelle Alves MD a ,
Thierry Perez MD b , Daniel Mathieu Pr a
a
Department of Respiratory and Critical Care Medicine, Calmette Hospital, Lille II University Hospital, Lille, 59000, France
b
Department of Lung Function, Calmette Hospital, Lille, 59000, France

Keywords:
Abstract
Chronic obstructive
Purpose: The aim of this study was to evaluate the manual compression of the abdomen (MCA) during
pulmonary disease;
expiration as a simple bedside method to detect expiratory flow limitation (EFL) during daily clinical
Dynamic pulmonary
practice of mechanical ventilation (MV).
hyperinflation;
Methods: We studied 44 semirecumbent intubated and sedated critically ill patients. Flow-volume loops
Expiratory flow limitation;
obtained during MCA were superimposed upon the preceding breaths and recorded with the ventilator.
Intrinsic positive end-
Expiratory flow limitation was expressed as percentage of expiratory tidal volume without any increase
expiratory pressure;
in flow during MCA (MCA [%VT]). In the first 13 patients, MCA was validated by comparison with the
Mechanical ventilation
negative expiratory pressure (NEP) technique. Esophageal pressure changes during MCA and intrinsic
positive end-expiratory pressure were also recorded in all the patients.
Results: Manual compression of the abdomen and NEP agreed in all cases in detecting EFL with a bias
of −0.16%. Percentage of expiratory tidal volume without any increase in flow during MCA is highly
correlated with percentage of expiratory tidal volume without any increase in flow during NEP (n = 13,
P b .0001, r2 = 0.99) and intrinsic positive end-expiratory pressure (n = 44, P b .001, r2 = 0.78), with a
good repeatability (n = 44; within-subject SD, 5.7%) and reproducibility (n = 13; within-subject SD,
2.41%). Two third of the patients were flow limited, among whom one third had no previously known
respiratory disease.
Conclusions: Manual compression of the abdomen provides a simple, rapid, and safe bedside reliable
maneuver to detect and quantify EFL during mechanical ventilation.
© 2012 Elsevier Inc. All rights reserved.

1. Introduction

All authors have read the manuscript and declare no financial In many respiratory diseases such as chronic obstructive
support, no potential conflict of interest, no prior publication or concurrent pulmonary disease (COPD), the destruction of lung paren-
submission, and no copyright constraints. chyma is responsible for a loss of the alveolar septa that
⁎ Corresponding author. Service de Réanimation Polyvalente, Hôpital
Calmette, Bd du Pr Jules Leclercq, 59000 Lille, France. Tel.: +33 3 20 44 44
normally support the small airways and keep them open [1].
95; fax: +33 3 20 44 50 94. As a result, the more the pleural pressure increases, the more
E-mail address: malcolmlemyze@yahoo.fr (M. Lemyze). poorly supported airways are compressed during expiration.

0883-9441/$ – see front matter © 2012 Elsevier Inc. All rights reserved.
doi:10.1016/j.jcrc.2011.05.011
38 M. Lemyze et al.

This dynamic compression of the small airways during mass index (BMI) above 30 kg/m2 was classified as obesity
expiration makes it impossible for the subject to increase its according to the World Health Organization's criteria [18].
expiratory flow beyond its resting value [2]. This phenom- The protocol was approved by the local ethics committee,
enon contributes to expiratory flow limitation (EFL). It leads and informed consent was obtained from the patients or next
to dynamic pulmonary hyperinflation promoting airway of kin.
closure, air trapping, and intrinsic positive end-expiratory
pressure (PEEPi) [3]. Dynamic pulmonary hyperinflation has 2.2. Measurements' conditions
deleterious consequences on the respiratory and circulatory
systems. From a respiratory point of view, it increases work The patients, placed in the semirecumbent position (upper
of breathing [4], impairs inspiratory muscle function [5], and half of the bed raised by 45°), were intubated with a cuffed
is one of the main mechanisms explaining dyspnea in patients endotracheal tube (Mallinckrodt, Athlone, Ireland) with inner
with COPD [6]. During mechanical ventilation (MV), it is diameter varying from 7.0 to 8.5 mm. All of them were lightly
associated with patient-ventilator asynchrony, delaying sedated with midazolam and remifentanyl according to the
weaning from the ventilator [7] and discharge from the protocol used in our ICU. Infusion rate was adapted by the
intensive care unit (ICU) [8]. It can also lead to detrimental nursing team on the Ramsay sedation scale to obtain a 3
hemodynamic effects such as depressed cardiac output and sedation level [19]. Controlled MV (Evita 2 dura or Evita 4;
reduced peripheral blood flow [3]. Gay et al [9] previously Dräger, Lübeck, Germany) was performed using a volume-
showed that detection of EFL during MV was a key controlled mode, delivering constant flow during insuffla-
information because the effect of positive end-expiratory tion. Baseline ventilatory settings were kept constant
pressure (PEEP) on respiratory system mechanics depends on throughout the experiment. For all patients, PEEP was
the presence or not of EFL. Therefore, many methods are put initially set to 0 on the ventilator. Airway pressure (Paw),
forward to detect EFL in mechanically ventilated patients: flow (V̇ ), and volume (V) were measured with the ventilator
removal of external PEEP, if present [10]; addition of built-in pressure transducer and flowmeter connected to a
resistances to the expiratory circuit of the ventilator [11]; personal computer. VentView 2.n software (version 01.01;
forced oscillation technique [12]; and application of negative Dräger Medizintechnick, Lübeck, Germany) enabled acqui-
expiratory pressure (NEP) at the airway opening during sition and continuous recording of Paw, V, and V̇ signals.
expiration [13]. However, none of them are easy to achieve in Expiratory muscle relaxation was confirmed by uniform
daily clinical practice, especially for critically ill patients sequential recordings of Paw, V, and V̇ and absence of
receiving MV. We investigated a simple bedside maneuver, negative deflections of Paw or other visible signs of patient-
the manual compression of the abdominal wall (MCA), ventilator asynchrony. Arterial blood gases were measured
already validated in spontaneously breathing patients with with a blood gas analyzer (ABL 725; Radiometer, Copenha-
COPD [14], to assess EFL in mechanically ventilated patients gen, Denmark) that was calibrated several times a day.
in the ICU by comparison with the NEP.
2.3. Respiratory mechanics

2. Methods Static PEEPi (PEEPi,stat) was determined using the end-


expiratory occlusion maneuver as previously described in
2.1. Eligibility detail [11].

Patients admitted in a 10-bed ICU of a tertiary university 2.4. Manual compression of the
hospital for any medical reason requiring invasive MV and abdomen maneuvers
sedation were prospectively included from December 2007
to April 2008. Manual compression of the abdomen was achieved as
The exclusion criteria were current pregnancy; recent described by Ninane et al [14] by a single investigator. He put
abdominal surgery; or any acute intra-abdominal disease, his right hand on the abdominal wall, with the palm on the
hemodynamic instability, severe hypoxemia defined as umbilicus oriented perpendicularly to the axis between the
PaO2/FIO2 less than 200, and presence of patient- xyphoid process and the pubis. After a short period allowing
ventilator asynchrony. recognition of the expiratory phase, the investigator exerted,
Anthropometric data, medical history of respiratory as soon as the insufflation was finished, a firm but gentle
disease, risk of death assessed by the Simplified Acute compression of the abdomen in an anteroposterior direction.
Physiology Score 2 [15], and duration of MV were recorded. This compression was maintained throughout expiration. To
Diagnosis of COPD was based on criteria detailed in the ensure that the maneuver was associated with an increase in
GOLD [Global Initiative for Chronic Obstructive Lung the expiratory-driving pressure, esophageal pressure and Paw
Disease] guidelines [16]; asthma was defined according to were continuously recorded at a digitizing frequency of 100
the Global Initiative for Asthma guidelines [17]. A body Hz. A saline solution–filled nasogastric tube and the filter of
MCA to assess EFL during MV 39

the endotracheal tube were each therefore connected to a expiratory flow during MCA was higher than under control
transducer and pressure analyzer [20]. Appropriate placement conditions, the subject was classified as having no EFL
of the esophageal tube was verified by recording small (Fig. 1). The FL portion was expressed as a percentage of
pressure variations synchronous to heart rate, confirming its the tidal volume and was called MCA (%VT). Its value
position behind the left atrium [21]. corresponds to the average of 3 consecutive measurements.
The V̇-V loops obtained during MCA maneuver and the
immediately preceding breaths were superimposed and
recorded via the ventilator. The first one acts as the control 2.5. Negative expiratory pressure method
curve. Patients were considered as flow limited (FL) when
all or part of the expiratory V̇-V curve during MCA were The endotracheal tube was connected through a low
superimposed on the control curve. On the contrary, if the resistive filter to a Hyp'air Compact pneumotachograph

Fig. 1 Comparison of the superimposed flow-volume (V-̇ V) loops obtained, respectively, with the MCA (on the left) and with the NEP
technique (on the right) for 2 patients. Expiratory phase is shown on the upper part of the curves, and insufflation phase is at the bottom. For
NFL patient 1, MCA and NEP both demonstrate a normal increase in flow during the whole expiration. Conversely, for FL patient 7, the
expiratory part of the V̇-V loops achieved with NEP as with MCA rapidly meet the control V̇-V loops, defining EFL. exp indicates expiratory
phase; ins, insufflation phase.
40 M. Lemyze et al.

MCA maneuvers were successively done in each of the 44


patients by the same investigator.
Results were expressed in mean ± SEM. Correlation
between EFL values, obtained by MCA and NEP, respec-
tively called MCA (%VT) and NEP (%VT), was performed
with Pearson rank correlation test (SPSS for Windows 9.0
[Chicago, IL, USA]). The graphic method described by
Bland and Altman [22] was used to compare the first
measure of MCA and NEP by plotting the differences
between the 2 techniques against their averages (Fig. 2).
Using a 1-way analysis of variance for repeated measures,
Fig. 2 Concordance analysis plots showing bias (thick line) and repeatability was assessed by calculating the within-subject
limits of agreement (dashed lines) between the 2 methods, MCA SD (SDw) corresponding to the square root of average
and NEP. Within the 13 patients, 6 are plotted at the point (0,0). variance of the 3 consecutive measures of MCA (%VT) in the
44 patients [23]. Repeatability of MCA-induced esophageal
pressure change (ΔPes) performed by a single investigator
(Medisoft, Dinan, Belgium) and a T tube with a 15-mL dead and reproducibility of MCA maneuvers between the 5
space. Assessment of EFL using the NEP technique was investigators in the first 13 patients were assessed using the
achieved as previously described with a negative-pressure same method. Nonparametric Mann-Whitney U test was
source set at −5 cm H2O by an observer blinded for MCA used to compare the quantitative variables within FL and
maneuver results [13]. V̇-V curve recorded during the NEP non-FL (NFL) patients, whereas Fisher exact test was used
maneuver was superimposed upon the preceding breath. for qualitative variables. For all tested variables, P b .05
Expiratory flow limitation was expressed as percentage of were considered statistically significant.
expiratory tidal volume during which no increase in flow was
found. Three consecutive measurements were performed in
each of the tested patients. 3. Results

We have studied 44 patients (28 men) 56 ± 2.6 years old


2.6. Study design and data analysis (minimum, 22; maximum, 87). Their main clinical charac-
teristics are summarized in Table 1. They had been under
Expiratory flow limitation was both assessed by MCA and MV for 4.7 ± 0.8 days (minimum, 1; maximum, 22). Mean
NEP in the first 13 patients enrolled. To assess reproducibility Simplified Acute Physiology Score 2 was 41.7 ± 1.9
(interobserver variation) of the MCA maneuver in these 13 (minimum, 15; maximum, 74). Twenty of them had a
patients, MCA was successively carried out by 5 investigators medical history of bronchial disease, diagnosed as COPD for
who had never been accustomed to the maneuver before the 17 of them and as asthma for 3 of them. Mean BMI reached
study. To evaluate repeatability (intraobserver variation), 3 29.6 ± 1.2 kg/m2, and 21 patients were classified as obese.

Table 1 Respiratory parameters of the 13 patients tested with MCA and NEP
Patient number VT RR TE PaO2/Fio2 PEEPi,stat NEP MCA ΔPes
(L) (breath/min) (sec) (cm H2O) (%VT) (%VT) (cm H2O)
1 0.55 18 2.53 496 0.4 0 0 8.9
2 0.5 18 2.63 317.5 0.5 0 0 10.7
3 0.5 18 2.63 474 1.2 0 0 13
4 0.5 20 2.30 262.5 1.2 0 0 7.9
5 0.5 20 2.35 242.5 1.2 0 0 10.6
6 0.5 18 2.68 547 0.8 0 0 12.5
7 0.55 18 2.63 242.5 4.9 48.7 44.4 7.2
8 0.5 18 2.53 463 6.2 56.3 56.6 20.3
9 0.5 18 2.68 389 3.1 63 59.2 14
10 0.55 24 1.70 326 10.0 87.7 82.6 15.4
11 0.4 18 2.78 370 15.2 90.3 84.9 34.3
12 0.5 16 3.1 255 16.2 97 88 19
13 0.5 18 2.68 411 5.9 87.3 90.6 24.4
VT indicates tidal volume; RR, respiratory rate; TE, expiratory time.
MCA to assess EFL during MV 41

3.1. Validation of MCA Table 2 Comparison of the NFL with the FL patients
Parameters NFL (n = 13) FL (n = 31) P
Respiratory characteristics of the 13 patients who were
Age (y) 40.6 ± 4 62.4 ± 2.5 b.001
tested with MCA and NEP maneuvers are presented in
Male (%) 10 (76) 18 (58) NS
Table 1. A significant correlation was found between EFL, BMI 23.9 ± 1.1 32 ± 1.5 b.001
quantified by MCA, called MCA (%VT), and EFL Obesity (n) 1 20 b.001
measured with the NEP technique, NEP (%VT) (n = 13, Previous smokers (n) 3 25 b.001
r2 = 0.99, P b .01). There was a perfect agreement COPD (n) 0 17 b.001
regarding the presence or absence of EFL between NEP Asthma (n) 0 3 b.001
and MCA. No patient without EFL recorded by NEP was SAPS 2 36.5 ± 4.1 43.8 ± 2.1 NS
FL as assessed by MCA and inversely. As shown in Figs. 2 Duration of MV (d) 10.5 ± 1.6 23.7 ± 4.2 .05
and 3, quantitatively, agreement between the 2 techniques ETT ID (mm) 7.5 ± 0.09 7.4 ± 0.07 NS
was also very good (n = 13; bias, −0.16% ± 3.9%; 95% VE (L/min−1) 9.4 ± 0.2 9.1 ± 0.2 NS
RR (breath/min−1) 18.8 ± 0.4 19.2 ± 0.3 NS
limits of agreement, −7.8%-7.5%). There was a clinically
TE (s) 2.5 ± 0.07 2.4 ± 0.05 NS
acceptable repeatability of MCA (%VT) in each subject
VT (mL/kg−1) 7.3 ± 0.27 8.2 ± 0.26 .03
(n = 44; SDw, 5.7%; P = .33). Despite large variations of PEEPi,stat (cm H2O) 0.9 ± 0.1 7.7 ± 0.7 b.0001
the esophageal pressure among the 5 investigators (n = 13;
SAPS 2 indicates Simplified Acute Physiologic Score 2; ETT ID,
SDw, 4.09 cm H2O; P b .0001), reproducibility of MCA endotracheal tube internal diameter; VE, minute ventilation.
(%VT) was also good (n = 13; SDw, 2.41%; P = .67).
No complication happened during the study because of
the MCA maneuver. noninvasive, bedside method to detect and quantify EFL
during MV and (2) MCA may easily reveal EFL in many
3.2. Comparison of the NFL (n = 13) with the FL ventilated patients in ICU, especially in patients without any
patients (n = 31) previously known respiratory disease.
Expiratory flow limitation assessment by the method
Among the 44 patients, 31 had EFL. All patients with a originally described by Hyatt [2] in 1961 and based on the
medical history of obstructive respiratory disease and all but comparison of the resting V̇-V curve with those obtained by a
1 of the 21 obese patients were FL. Eleven FL patients had forced vital capacity maneuver is not appropriate for patients
no previously known respiratory disease. Only 4 patients in the ICU. First, because of the gas compression during the
demonstrated EFL without COPD, obesity, or asthma. Main forced vital capacity maneuver, volumes have to be
clinical and physiologic characteristics of FL patients measured in a plethysmography cabin [24]. Second,
compared with NFL patients are shown in Table 2. Fig. 4 expiratory flow depends on the volume and time history of
illustrates that PEEPi,stat correlates well with MCA (%VT) the preceding breath [25]. Because volume and time history
(n = 44, r2 = 0.78, P b .0001). Note that none of the patient are very different between the resting inspiration and the one
with PEEPi less than 1.6 cm H2O demonstrated EFL. obtained during forced vital capacity maneuver, EFL
detection by the comparison of the resting V̇-V loop with
the maximal one often leads to erroneous conclusions.
4. Discussion Finally, expiratory flow during a forced vital capacity
maneuver through an endotracheal tube is clearly limited
The main results of the present study could be by the diameter of the tube [26].
summarized as (1) MCA appears to be a simple, safe,

Fig. 4 Correlation between dynamic pulmonary hyperinflation,


Fig. 3 Comparison between FL volume assessed by MCA and assessed by PEEPi,stat, and EFL, assessed by percentage of FL tidal
NEP in 13 patients showing very similar results. volume during MCA(%VT) (n = 44, P b .0001, r2 = 0.78).
42 M. Lemyze et al.

To avoid these numerous pitfalls, another technique, the obstructive respiratory disease. Among the 44 patients of the
application of an NEP, has been introduced and validated present study, 11 matched these criteria. Some of them are
during MV by concomitant determination of isovolume elderly or obese patients. Closing volume is known to
flow-pressure relationships [13]. The NEP technique does increase linearly with advancing age, especially in the supine
neither require performance of forced vital capacity position [27]. In addition, half of our population consisted of
maneuvers from the patient nor a body plethysmograph. obese patients, and all but 1 presented EFL. Low tidal
Although NEP method is a noninvasive technique specially volume ventilation of obese subjects promotes small airways
fitted for subjects receiving MV, it requires an expensive occlusion and EFL leading to dynamic pulmonary hyperin-
material added on the ventilator [13]. flation and PEEPi, especially in the supine position [28].
In this study, MCA, a much simpler method, was Regardless of age and weight, EFL may develop as an acute
compared with NEP, considered as a reference method to condition during MV because of the reduction of the
detect EFL. During MV, MCA mimics a forced expiratory bronchial caliber. Two of them—a 45-year-old man and a
maneuver that results in an increased pressure gradient 48-year-old woman, both nonsmokers—had initially re-
driving the expiratory flow, with strictly superimposable ceived large amount of fluid because of septic shock caused
conditions regarding the preceding control breath. This by extensive cellulitis. In an 87-year-old woman with a
lasting characteristic of the MCA technique allows the medical history of congestive heart failure and admitted to
method to be freed from the limits discussed above. A the ICU for septic shock, EFL may result, at least in part,
limitation of this study may be the small number of patients. from her great age and acute pulmonary edema. In the last
However, to our knowledge, none of the previously validated one—a 44-year-old man who developed postanoxic enceph-
methods of EFL assessment have been conducted in a greater alopathy after an attempted suicide by hanging—no
number of ventilated patients [11,13]. In the ICU, MCA is causative factor can be isolated. Indeed, bronchial edema
really easy to achieve in the real conditions of the daily may be present in critically ill patients who received large
clinical practice of MV because the only device it needs is a amounts of fluid during the initial resuscitative period of
ventilator. Indeed, most modern ventilators used in the ICU sepsis but also because of sepsis-associated acute lung injury
are equipped with a reliable pneumotachograph, and super- or ventilator induced lung injury [29]. Manual compression
imposed flow-volume loops can be directly displayed on the of the abdomen may be useful as a quick and simple
ventilator screen. Manual compression of the abdomen does technique to detect EFL especially when the clinician would
not require collaboration from the patient, which is an not have expected the patient to be FL.
essential condition for any method of measurements used in Intrinsic PEEP measured in static conditions (with end-
critically ill patients. However, it may be argued that MCA expiratory occlusion maneuver) overestimates the one
lacks standardization. The agreement between the results measured in dynamic conditions during MV [30]. Abnormal
obtained with MCA and NEP methods and the high contraction of the abdominal muscles during expiration, even
correlation between EFL magnitude determined by the 2 clinically undetectable, may overestimate dynamic PEEPi
methods ensures that MCA-assessed EFL is reliable. In our value [31]. Although both palpation of the abdominal wall
study, change in esophageal pressure value (ΔPes) resulting attested relaxation of the expiratory muscles and stable
from MCA was not reproducible from a maneuver to another pressure, volume, flow curves, and a plateau in Paw were
even when performed by the same investigator on the same constantly observed in our study, postinspiratory muscle
patient. Nevertheless, the level of EFL taken as MCA (%VT) contraction cannot be totally ruled out. This may explain the
from 1 maneuver to another in the same subject remains with greater dispersion of measured PEEPi,stat value from those
a clinically acceptable repeatability and reproducibility predicted by the regression equation using MCA (%VT) in
whatever the real level of the ΔPes achieved. Provided that the patients with the most severe EFL. However, none of the
a minimal driving pressure is achieved by either an NEP or a patients with measured PEEPi,stat below 1.6 cm H2O had
MCA, the same results are obtained in terms of detection and EFL. Consequently, when a patient shows no pulmonary
titration of EFL. Manual compression of the abdomen has the hyperinflation as demonstrated by a PEEPi approaching 0, it
definite advantages of being quicker, as effective and cheaper is likely that looking for EFL is useless. In that case, MCA
than the NEP technique because it requires no special device should not be performed.
added to the ventilator and no adjustments of the ventilator Conversely, whenever dynamic pulmonary hyperinflation
settings. Finally, MCA can easily be achieved without the use is suspected during MV, detection of EFL is paramount
of muscle relaxant. On the contrary, MCA has been because EFL may lead to incomplete lung emptying and
successfully applied in spontaneously breathing subjects promotes end-expiratory air trapping. In our study, EFL was
[14]. In consequence, MCA should also be applicable during constantly present when PEEPi,stat exceeded 1.6 cm H2O.
any type of triggered MV such as pressure support. Detection of EFL is a real challenge and enables to
Expiratory flow limitation is a hallmark finding of distinguish 2 different clinical situations. First, dynamic
patients with obstructive lung disease [2]. But one interesting pulmonary hyperinflation without EFL often results from
finding in our study is that some critically ill patients inappropriate ventilator settings [32]. In that case, the simple
demonstrate EFL during MV without any previously known reduction of the tidal volume or increase in expiratory time
MCA to assess EFL during MV 43

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