Hindawi Publishing Corporation
Volume 2013, Article ID 749860, 6 pages
Expiratory Flow Limitation Definition, Mechanisms,
Methods, and Significance
Department of Experimental and Clinical Sciences, University of Brescia, 1a Medicina, Spedali Civili, 25123 Brescia, Italy
Correspondence should be addressed to Claudio Tantucci; email@example.com
Received 6 November 2012; Accepted 24 December 2012
Academic Editor: Kiriakos Karkoulias
Copyright © 2013 Claudio Tantucci. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
When expiratory flow is maximal during tidal breathing and cannot be increased unless operative lung volumes move towards
total lung capacity, tidal expiratory flow limitation (EFL) is said to occur. EFL represents a severe mechanical constraint caused by
in obstructive lung diseases and particularly in chronic obstructive pulmonary disease (COPD). Although in COPD patients EFL
more commonly develops during exercise, in more advanced disorder it can be present at rest, before in supine position, and then
in seated-sitting position. In any circumstances EFL predisposes to pulmonary dynamic hyperinflation and its unfavorable effects
to reduced exercise tolerance, marked breathlessness during effort, and severe chronic dyspnea.
Expiratory (air) flow limitation (EFL) during tidal breathing
is a well-defined, mechanical pathophysiological condition
occurring, either during physical exercise or at rest, before
in supine and later on in sitting-standing position, when
expiratory flow cannot be further increased by increasing
expiratory muscles effort (i.e., by increasing pleural and
. In other words, under the prevailing conditions, the
respiratory system is globally limited as flow generator even
during tidal expiration, and greater expiratory flow rates
may be achieved just by increasing operating lung volumes,
(i.e., moving progressively the end-expiratory lung volume
(EELV) towards total lung capacity). In fact, the volume-
related decrease of airway resistance and increase of elastic
recoil are the only effective mechanisms to obtain higher
expiratory flows in case of EFL .
rates at a given lung volume, as compared to predicted (i.e.,
airflow reduction or airflow obstruction), is inappropriate
and should not be adopted unless the condition previously
described is present (Figure 1).
2. Mechanisms of EFL
Several mechanisms may contribute to the EFL development
by reducing the expiratory flow reserve in the tidal volume
The age-related increment of closing volume and closing
capacity may induce in the elderly the closure of dependent
flow rates corresponding to tidal volume . Actually, the
lung senescence may predispose to EFL, especially in the
supine position and in small sized, overweight women.
When supine, the relaxation volume of the respiratory
system (푉푟) is lower as a result of gravitational forces, and
assuming the supine position , this body position predis-
poses to EFL because tidal breathing occurs at lower lung
volumes where maximal expiratory flow rates are necessarily
Breathing at low-lung volume (near residual volume), as
frequently observed in great and massive obesity, chronic
congestive heart failure, and sometimes in restrictive lung
and chest wall disorders, intrinsically reduces the maximal
usually EELV decreases with recumbency . Since the
maximal flow-volume curve denotes minimal variation by
2 Pulmonary Medicine
EFL at rest
Flow rate (L/s)
No EFL at rest
Flow rate (L/s)
Flow rate (L/s)
Flow rate (L/s)
Figure 1: Maximal and tidal flow-volume curve in two representative COPD patients: one with airflow reduction and tidal expiratory flow
limitation (EFL) at rest (a), the other only with airflow reduction at rest and potential EFL during exercise (b). The NEP application at rest
does not increase expiratory flow in the first patient (c), while eliciting greater expiratory flow in the second one (d).
EFL occurrence, mainly in the supine position.
Higher ventilatory requirements with larger tidal volume
(for similar respiratory rate and expiratory time), faster
respiratory rate and shorter expiratory time (for similar tidal
volume), or both, as expected during exercise or observed
even at rest in various conditions, do increase mean tidal
expiratory flow and reduce expiratory flow reserve during
tidal breathing, making easier to have EFL.
On the other hand, EFL is linked inescapably to the
presence of airflow reduction, no matter what is the pre-
vailing mechanism (increased airway resistance, augmented
cholinergic bronchial tone, decreased lung elastance, airway-
parenchyma uncoupling, and airways collapsibility) in the
obstructive lung diseases such COPD (Figure 2), chronic
asthma, cystic fibrosis, constrictive bronchiolitis [6, 7]. In
this respect, predominant reduction of maximal expiratory
flow rates at lower lung volumes appears more crucial in
promoting EFL. However, the site where the system becomes
entirely flow-limited and flow limiting segment develops can
be located centrally or peripherally. When EFL originates
in the peripheral airways, it is mainly due to the viscous,
density-independent, flow-limiting mechanism, while the
speed wave, density-dependent, flow-limiting mechanism is
Therefore, aging, body position, exercise, hyperpnea-
tachypnea, low-volume breathing, or airflow reduction rep-
resents, alone or more often combined together, the main
factors that favor the development of EFL in humans.
Alveolar pressure (+)
65% of exp. FVC
Alveolar pressure (−)
Tidal expiratory flow limitation
Δ푃 = 푃alv− 푃pl= 푃el
Δ푃 = 푃alv− 푃ao
푃pl: pleural pressure
푃crit: critical pleural pressure
푃alv: alveolar pressure
푃ao: airway opening pressure
푃el: elastic recoil pressure
Figure 2: Isovolume (low-lung volume) flow-pressure relationship
and COPD with expiratory flow limitation (FL). In any case, after
푃crit, expiratory flow does not increase further on, and its driving
tidal volume range.
3. Methods for EFL Detection
Classically, flow limitation may be detected looking at iso-
volume pleural (or alveolar) pressure-flow relationship, and
it occurs, when expiratory flow rate does not change (or
even is reduced) despite the increasing pleural (alveolar)
pressure . Therefore, if increasing pleural pressure at
lung volume corresponding to tidal breathing induces no
change in expiratory flow, EFL is documented. Comparison
between full (or partial) maximal and resting flow-volume
loops has been used to detect EFL which is assumed when
expiratory tidal flow impinges on or is even greater than
maximal expiratory flow at the same lung volume .
This method that, however, should be performed by body
plethysmography to avoid artifacts due to the thoracic gas
compression  is fatally flawed by the sequential emptying
in the preceding inspiration [12, 13]. In fact all these factors
influence the corresponding expiratory flow rates that are
going to be compared in the two maneuvers. To respect time
to limit (or avoid by using body plethysmography) thoracic
gas compression, comparison between submaximal (i.e.,
with gentle expiratory effort) and resting tidal flow-volume
curve has been suggested for assessing EFL. Obviously this
technique demands high cooperation and uncommon ability
from the patients and cannot be standardized.
More than 15 years ago, to overcome all these problems,
the Negative Expiratory Pressure (NEP) method has been
introduced in the research and clinical practice . A
at the mouth at the beginning of expiration to establish a
pressure gradient between the alveoli and airway opening.
During NEP that lasts for the whole expiration, there is an
increase in expiratory flow in the absence of EFL, while
the expiratory flow does not increase over the flow of the
preceding control expiration, throughout the entire or part
of the tidal expiration, in the presence of (total or partial)
EFL (Figure 1). The NEP method that has been validated by
using isovolume pressure-flow curves  does not require
cooperation from the subjects and use of body plethys-
mography, can be performed at rest in any body position
and during effort, and usually is devoid from interpretative
induced by the NEP application, as observed in snorers and
OSAH patients, that can be partially controlled by reducing
the negative pressure and repeating the measurements. The
however, lead to unclear results by using this technique.
This inconvenience is absent during the manual com-
pression of abdominal wall (CAM) that, performed at rest
or during exercise simultaneously with the start of tidal
of the preceding control expiration in the absence of EFL. In
indicates EFL . The ability of the physician or technician,
the cooperation of the patients, and the glottic reflex possibly
elicited by this maneuver that cannot be standardized limit
the utility of CAM for assessing EFL.
Recently the use of forced oscillation technique (FOT)
during tidal breathing has been used to detect EFL breath-
by-breath, both at rest and during exercise . Briefly, when
the oscillatory pressure applied at the mouth does not reach
the alveoli during expiration because a flow limiting segment
reflecting the mechanical properties of the lung parenchyma
and airways, is influenced only by those of the airways and
becomes much more negative with a clear within-breath dis-
tinction between inspiration and expiration. This application
of the FOT is very promising to identify EFL during tidal
breathing, but the closure of intrathoracic airways eventually
occurring at EELV must be considered as an important
reactance signal is similar.
4. EFL, Dynamic Hyperinflation, and Dyspnea
The development of EFL is functionally relevant because
either in the supine or seated position) EFL is associated or
for a given expiratory tidal volume, the time required for the
respiratory system to reach its relaxation volume (푉푟) .
often dynamically raised  and invariably increases with
respiratory rate) . When EFL develops during exercise,
EELV starts to increase and inspiratory capacity to decrease,
Indeed, in the presence of EFL at rest, although DH can be
avoided if the expiratory time is long enough, EELV is more
4 Pulmonary Medicine
both signaling the occurrence of progressively greater DH
DH promotes neuromechanical dissociation and implies
a positive alveolar end-expiratory pressure (PEEPi) with a
concomitant increase in inspiratory work, due to PEEPi act-
These factors together with dynamic airway (downstream
from the flow-limiting segment) compression during expira-
tion may contribute to the dyspnea sensation [23, 24].
5. Clinical Aspects
In healthy subjects EFL occurs neither at rest nor during
strenuous exercise , with the exception of highly fit old
individuals in whom EELV tends to increase at high levels of
exercise because of elevated values of minute ventilation they
can reach before stopping . Since maximal expiratory
flow rates are reduced near EELV because of lung volume
functional reduction due to age-related increase of closing
capacity, EFL may develop under these circumstances .
Recently, however, for the same reasons EFL has been found
by using the NEP technique also at rest in a large number
of very old subjects, especially in small sized elderly women.
Among these aged subjects chronic dyspnea was frequently
EFL may occur during tidal breathing at rest in COPD
with moderate-to-severe-to-very-severe airway obstruction
[6, 14, 19, 28]. Despite this general picture, changes in
conventional indices of airway obstruction such as FEV1,
curve are not useful to predict EFL, and special techniques
dyspnea better than routine spirometric parameters . In
risk of dynamic pulmonary hyperinflation (DH), and DH
has been recognized as an important cause of dyspnea either
work of breathing, inspiratory muscle function, and, above
all, neuromechanical coupling [21, 23].
It has been postulated that, in COPD for similar degrees
of airflow obstruction, as measured by FEV1reduction as
during exercise and at rest, in patients with emphysematous
phenotype in whom reduction of lung elastic recoil and
to be the main determinants of airflow reduction. Under
these conditions the peripheral small airways should be
more compliant and prone to collapse during expiration
favoring EFL that might partly explain the greater dyspnea
patients with moderate-to-severe airflow obstruction, EFL
assessed by the NEP technique was detected significantly
more in those with lower values of DLCOand KCO, but
only when appraised in the supine position, suggesting an
PEF, and FEV1/FVC derived from maximal flow/volume
percent predicted, EFL could be more easily observed, both
earlier appearance of EFL in emphysematous COPD patients
(Figure 3). Interestingly, in these patients, chronic dyspnea,
as measured by the modified MRC scale, was significantly
this observation than links supine EFL and emphysema
During episodes of acute exacerbation and respiratory
failure, COPD patients are prone to develop DH even in
the absence of EFL because of increase in airway resistance
with longer time constant in the respiratory system and
rapid and shallow breathing with reduction of expiratory
time . Moreover, higher ventilatory requirements due
to fever and/or anxiety, increased physiological dead space,
and deterioration of gas exchange may contribute to DH.
In the presence of EFL, however, all these factors cause a
catastrophic increase in DH that cannot be longer sustained
during spontaneous breathing without unbearable dyspnea
acute ventilatory failure (ARF) and adoption of mechanical
ventilation . With this regard, it should be stressed
that almost all COPD patients mechanically ventilated for
ARF exhibit EFL, since further increase in expiratory flow
resistance is induced by endotracheal tube and expiratory
circuit of the ventilator . This is relevant when assisted
stances the inspiratory work could be very high yet, and the
application of PEEP to counterbalance PEEPi can reduce the
elastic threshold load without increasing EELV.
Conversely, apart from patients with severe chronic
obstruction , EFL at rest is seldom observed in asth-
matic patients, unless under severe and prolonged broncho-
In clinically stable patients with restrictive ventilatory
disorders EFL is very uncommon during tidal breathing at
In obese subjects and in patients with stable chronic
heart failure EFL at rest is rarely present in seated position.
However, recent studies showed that in massive obese sub-
heart failure of EFL was frequently detected in the supine
position [34, 35]. In all instances the development of EFL
with recumbency prevents EELV to reach supine 푉푟, leading
occurrence of supine EFL may be associated with the onset
of orthopnea either in massively obese subjects and patients
with chronic heart failure [34, 35].
to supine DH with concomitant PEEPi. Since this elastic
threshold load imposed to shorter (and functionally weaker)
occurs in COPD patients, even with mild-to-moderate air-
flow obstruction, during exercise, fatally inducing the onset
of DH and its progressive worsening, with the well-known
negative mechanical, muscular, cardiovascular, and symp-
tomatic consequences. Even worse in the natural history of
NFL supineFL supine
NFL supineFL supine
NFL supineFL supine
NFL supine FL supine
IC predicted (%)
emphysematous patients are more prone to develop recumbent EFL.
(FL; 푛 = 14) versus those who do not (NFL; 푛 = 13). Both DLCOand KCOare significantly lower in FL patients (∗푃 < 0.05), suggesting that
COPD is the presence of EFL at rest, initially only in the
supine position, contributing to orthopnea (and probably to
more severe symptoms in early morning) in these patients
and subsequently in the sitting-standing position limiting
their daily physical activity and causing (very often) DH
during resting tidal breathing with persistent volume-related
mechanical stress in the lung parenchyma. Physicians who
take care of COPD patients should be aware of this severe
functional condition that, once established, rarely can be
reversed with the present educational, pharmacological, and
rehabilitative therapy and try to avoid it treating much
earlier and more aggressively airflow obstruction and its
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