Lung (2008) 186 (Suppl 1):S3–S6
DOI 10.1007/s00408-007-9036-8
Before We Get Started: What Is a Cough?
Giovanni A. Fontana
Received: 31 July 2007 / Accepted: 2 August 2007 / Published online: 2 October 2007
Ó Springer Science+Business Media, LLC 2007
Abstract Cough is an airway defensive reflex consisting
of an inspiratory phase followed by a forced expiratory
effort initially against a closed glottis, followed by active
glottal opening and rapid expiratory flow. The expiration
reflex (ER) differentiates from cough for the lack of a
preparatory inspiration. The reflexes subserve different
functions: cough will clear the lower airways from debris
and mucus, while the expiration reflex will prevent aspi-
ration. Clinically, a cough epoch is a sequence of motor
acts resulting from a combination of true coughs and ERs
that need to be accurately identified and measured for
adequate quantitative description.
Keywords Cough
Expiration reflex
In the dictionary [1], cough is described as ‘‘a violent
expulsion of air from the lungs with a characteristic
sound,’’ a definition favored by many clinicians. A second
definition of cough, almost invariably preferred by physi-
ologists, is perhaps more complicated but certainly more
explanatory: cough is a three-phase expulsive motor act
characterized by an inspiratory effort (inspiratory phase)
followed by a forced expiratory effort initially against a
closed glottis (compressive phase), and then by active
glottal opening and rapid expiratory flow (expulsive
phase). Some recent guidelines [2] on the management of
cough have adopted exclusively the first definition, with
some important changes: ‘‘Cough is a forced expulsive
manoeuvre, usually against a closed glottis and which is
G. A. Fontana (&)
Department of Critical Care, University of Florence,
Viale G. B. Morgagni, 85, Florence 50134, Italy
e-mail: g.fontana@dac.unifi.it
associated with a characteristic sound.’’ Thus, according to
this definition, glottal closure would not necessarily be an
integral part of the cough reflex. Other guidelines on cough
assessment have adopted both definitions [3].
Another important difference between the ‘‘clinical’’
and ‘‘physiologic’’ definitions of cough is that only the
latter acknowledges the inspiratory phase of cough as being
a defining feature of the reflex. The inspiratory phase of
cough is important for at least two reasons: First, it allows
one to distinguish cough from another airway defensive/
protective reflex, the expiration reflex [4]; second, the
mechanical forces brought into action by the inspiration of
cough have a major impact on the intensity and effec-
tiveness of the subsequent expulsive effort [5].
The expiration reflex was first described by Williams in
1841 [6], and extensively studied by Korpas and colleagues
in the 1960s [4]. It may be evoked by mechanical or
chemical irritation of the vocal folds or trachea and consists
of a glottal closure and forced expiration followed by
glottal opening and expulsive airflow. Thus, compared to
cough, the expiration reflex lacks a preparatory inspiration.
The differences in pattern between cough and the expira-
tion reflex imply the activation of different neural
mechanisms and this has been confirmed by extensive
neurophysiologic studies [7, 8]. More importantly, the two
reflexes have different physiologic and pharmacologic
properties [4, 9] and appear to subserve quite different
functions: Cough will clear the lower airways of debris,
including mucus, while the expiration reflex will prevent
aspiration of material into the lungs. These differences
have been fully discussed elsewhere [9, 10].
Cough and the expiration reflex cooperate in defending
the lower airways but rarely occur in a pure or isolated
form. In practice, the ‘‘cough’’ often occurs in ‘‘epochs’’ or
‘‘bouts’’ [9]; a cough epoch represents a complex sequence
123
S4
of motor acts resulting from a combination of true coughs
and expiration reflexes [11, 12]. Different sequences of
expulsive efforts produced voluntarily or following stim-
ulation of various regions in the respiratory tract are
depicted in Figure 1.
Because the motor patterns of cough and the expiration
reflex are rather complicated, there are many variables that
may be measured. These include respiratory flow and
volume, respiratory muscle activity, respiratory pressures,
and, of course, cough frequency. Additional important
information can be obtained from the study of cough-
associated sensations [13]. Basically, the choice of what to
measure depends on what information is being sought. For
instance, if one wishes to assess whether a patient benefits
from a certain cough treatment, recordings of cough fre-
quency may suffice. Conversely, in analytical studies of
cough and its mechanisms, it is desirable to measure as
many of the above-mentioned variables as possible.
The most widely used method for assessing cough in the
clinical setting is the recording of its frequency, usually by
means of a microphone. There is no dispute that mea-
surements of cough frequency have contributed to our
knowledge, especially in the field of cough pharmacology.
Accordingly, the effectiveness of some cough sedatives
may be determined satisfactorily by simply recording
cough frequency. Nevertheless, it must be borne in mind
that the measurement of the variable has important limi-
tations. It treats all coughs as equal, i.e., it does not
consider the force developed during each expulsive effort,
and its determinants have not been established clearly.
Furthermore, cough frequency is not suitable for use in
differentiating between cough and expiration reflexes,
which brings us back to the core problem of a need to
precisely define what is a cough.
Fig. 1 A Voluntary coughs and a cough epoch in a female subject.
Traces (from the top): time (in s), cough sound, airflow (expiration
upwards), thoracic/esophageal pressure (positive upwards), and
abdominal pressure (positive upwards). On the left are two voluntary
coughs. They are followed by a spontaneous involuntary cough epoch
consisting of an initial inspiration and then four compressive and
expulsive phases without intermediate inspirations. Vertical lines
indicate equal time points (from [12]). B Respiratory response to
123
Lung (2008) 186 (Suppl 1):S3–S6
Another potential limitation of recording cough fre-
quency may be that the recording of cough sounds by a
listener is labor-intensive and probably impractical in
ambulatory conditions. For these reasons automated
audiometric methods have been devised [14–17]. The main
problem with audiometric methods is that currently
they record only expiratory efforts and therefore cannot
distinguish between cough and the expiration reflex. Fur-
thermore, the identified expiratory efforts cannot easily be
separated into those of isolated coughs and those in cough
epochs. However, these limitations are probably of little
relevance to most clinical studies. On the other hand, other
methods of assessing cough, by airflow, volume, respira-
tory pressure, and electromyographic (EMG) activity, will
also allow measurement of the frequency of all expulsive
efforts, either coughs or expiration reflexes.
The motor pattern of coughing involves the coordinated
activation of several muscles exerting their action on the
upper airways or chest wall. Upper airway muscles, espe-
cially those of the mouth and larynx, can greatly influence
airflow and their activation needs to be synchronized with
that of the respiratory muscles to control upper airway
patency and to produce the cough flow.
Activation of the inspiratory muscles (mainly the dia-
phragm and the external intercostals) during the
preparatory inspiration of cough has a major impact on
cough intensity. In his review on the physiologic and
pharmacologic properties of cough, Bucher [18] was
among the first to underline the importance of the cough
inspiratory phase: ‘‘We should therefore like to propose
that the inspiration immediately preceding the expiratory
thrust is an integral part of the act of coughing. It is an
important link between the stimulus and the resulting
response. The deeper the inspiration the stronger the
laryngeal stimulation by injection of distilled water (at arrow) in an
awake human subject. The injection was given via a nasal endoscope.
Pressure, airflow, and end-tidal CO2 tension were recorded via a face
mask. Note that there are three initial expirations (the ER) followed
by an inspiration and two expirations (the cough reflex) (from [11]).
C Same as in B but with the subject lightly anesthetized with propofol
(from [11])
Lung (2008) 186 (Suppl 1):S3–S6
expiratory thrust, under otherwise equal condition.’’ During
voluntary cough efforts, the inspiratory volume is related to
the anticipated forcefulness of the subsequent cough effort
(reviewed in [5]); however, little is known about the reg-
ulation of inspiratory volume during the inspiratory phase
of spontaneous cough. It may be related, at least in part, to
the intensity of the stimulus causing the cough (G. Fontana,
unpublished observations).
The expiratory muscles of the ventrolateral aspect of the
abdominal wall, such as the oblique (external and internal)
muscle, the tranversus abdominis, and the rectus abdominis
[19], are intensely activated during both the compressive
and the expulsive phases of cough [20] and the expiration
reflex [10]. EMG recordings of the expiratory muscles have
been used not only to study the neural mechanisms of
cough but also to assess its intensity [21–24]. It has been
shown that the rate of rise of the integrated EMG activity
reflects the rate of recruitment of motor units and of the
increase in their firing frequency, while the peak of the
integrated EMG activity is an expression of the total
number of units recruited and of their maximum firing
frequency [25]. Thus, EMG recordings of expiratory
muscle output during cough can provide insights into the
neural mechanisms activated during cough and during the
ER. Because the magnitude of EMG activity correlates
with the force produced by the contracting muscle [26],
recordings of EMG activity of human abdominal muscle
activity have been used to assess the intensity of induced
cough efforts (see [21] for further refs).
Inspiratory and especially expiratory airflows can be
measured easily and are therefore widely used in the
characterization of cough [21, 22, 24]. Measurements of
mouth pressure during coughing may also provide useful
information. Cough flow is regulated in the same way as
that of a forced expiration [5, 27]. Flow transients of a
magnitude exceeding that dictated by the pulmonary
pressure-flow relationships are commonly attained due to
compression of the airway walls during the cough expul-
sive phase [5, 27].
Measurements of cough flows and pressure at the mouth
level are not only relatively easy to perform but they also
provide a unique opportunity to evaluate the duration of the
cough compressive phase. In fact, during this phase, air is
compressed within the lungs due to the glottal closure and
simultaneous activation of the expiratory muscles. Thus,
mouth pressure and airflow drop to zero and become
positive only at the onset of the subsequent expulsive phase
[5, 27]. Interestingly, while it is well known that the cough
compressive phase lasts approximately 0.2 s [5, 27], it is
unclear if and to what extent compression time varies
according to the underlying cause of cough, and if the
duration of the compressive phase of the expiration reflex
is the same as that of cough.
S5
Lung volume changes associated with cough can be
measured either with a body inductance vest, or its
equivalent, or by integrating an airflow signal from the
mouth. Calibration of the inductance for accurately
recording the vigorous movements of the torso in coughing
may be labor-intensive; however, cough expiratory flow
and volume can be measured fairly accurately using a
calibrated pneumotachograph. Because the force developed
during the expulsions of cough largely depends on the
magnitude of the preceding inspiration [5, 18, 27], mea-
surements of cough inspiratory volume might also
represent a useful indicator of cough intensity.
In conclusion, researchers face two problems that are
related to each other: They need to define cough accurately
and, to do so, they must also be able to evaluate the dis-
tinctive features of cough and other respiratory reflexes,
particularly the expiration reflex. To accomplish this, and
to describe adequately the many facets of cough, the use of
techniques capable of quantifying the sensory-motor fea-
tures of cough and cough-like reflexes is highly
recommended.
Acknowledgments The author is grateful to Prof. John Widdi-
combe who has inspired many of the concepts presented in this
article.
References
1. Anonymous (1973) The Shorter Oxford English Dictionary 3rd
ed. Oxford: Clarendon Press, p 436
2. Morice AH, McGarvey L, Pavord I (2006) Recommendations for
the management of cough in adults. Thorax 61(Suppl 1):1–24
3. Morice AH, Fontana GA, Belvisi MG, Birring SS, Chung KF,
Dicpinigaitis PV, Kastelik JA, McGarvey LP, Smith JA, Tatar M,
Widdicombe J, European Respiratory Society (2007) ERS
guidelines on the assessment of cough. Eur Respir J 29:1256–
1276
4. Korpas J, Tomori Z (1979) Cough and Other Respiratory
Reflexes. Basel: Karger, pp 1–281
5. Leith DE (1977) Cough. In: Brain JD, Proctor DF, Reid LM (eds)
Respiratory defense mechanisms. New York: Marcel Dekker, pp
545–592
6. Williams CBJ (1841) Report of experiments on the physiology
of the lungs and air-tubes. Rep Br Assn Adv Sci August: 411–
420
7. Shannon R, Baekey DM, Morris KF, Nuding SC, Segers LS,
Lindsey BG (2004) Production of reflex cough by brainstem
respiratory networks. Pulm Pharmacol Ther 6:369–381
8. Baekey DM, Morris KF, Nuding SG, Segars LS, Lindsey BG,
Shannon R (2004) Ventrolateral medullary respiratory network
participation in the expiration reflex in the cat. J Appl Physiol
96:2057–2072
9. Widdicombe J, Fontana G (2006) Cough: what’s in a name? Eur
Respir J 28:10–15
10. Tatar M, Hanacek J, Widdicombe J (2007) The expiration reflex
from the trachea and bronchi. Eur Respir J (in press)
11. Nishino T, Tagaito Y, Isono S (1996) Cough and other reflexes
on irritation of airway mucosa in man. Pulm Pharmacol 9:285–
292
123
S6
12. Young S, Abdul-Sattar N, Caric D (1987) Glottic closure and
high flows are not necessary for productive cough. Bull Eur
Physiolpathol Respir 23(Suppl 10):13S–17S
13. Davenport PW, Sapienza CM, Bolser DC (2002) Psychophysical
assessment of the urge-to-cough. Eur Respir Rev 12:249–253
14. Hsu J-Y, Stone RA, Logan-Sinclair R, Worsdell M, Busst C, Chung
KF (1994) Coughing frequency in patients with persistent cough
using a 24-hour ambulatory recorder. Eur Respir J 7:1246–1253
15. Barry SJ, Dane AD, Morice AH, Walmsley AD (2006) The
automatic recognition and counting of cough. Cough 2:8
16. Morata A, Ohota N, Shibuya A, Ono H, Kudoh S (2006) New
non-invasive automatic cough counting program based on 6 types
of classified cough sounds. Intern Med 45:391–397
17. Smith J (2007) Ambulatory methods for recording cough. Pulm
Pharmacol Ther 20(4):313–318
18. Bucher K (1958) Pathophysiology and pharmacology of cough.
Pharm Rev 10:43–58
19. Strohl KP, Mead J, Banzett RB, Loring S, Kosch P (1981)
Regional differences in abdominal muscle activity during various
maneuvres in humans. J Appl Physiol 51:1471–1476
20. De Troyer A, Loring SH (1986) Action of respiratory muscles. In:
Handbook of Physiology. The Respiratory System. Mechanics of
Breathing. Bethesda, MD: Am Physiol Soc, sect 3, vol III, chap
27, pp 1–67
123
Lung (2008) 186 (Suppl 1):S3–S6
21. Fontana GA, Pantaleo T, Lavorini F, Boddi V, Panuccio P (1997)
A non-invasive electromyographic study on threshold and
intensity of cough in humans. Eur Respir J 10:983–989
22. Fontana GA, Pantaleo T, Lavorini F, Polli G, Pistolesi M (1999)
Coughing in laryngectomized patients. Am J Respir Crit Care
Med 160:1578–1584
23. Fontana GA, Pantaleo T, Lavorini F, Benvenuti F, Gangemi S
(1998) Defective motor control of coughing in Parkinson’s dis-
ease. Am J Respir Crit Care Med 158:458–464
24. Lavorini F, Pantaleo T, Geri P, Mutolo D, Pistolesi M, Fontana
GA (2007) Cough and ventilatory adjustments evoked by aeros-
olised capsaicin and distilled water (fog) in man. Respir Physiol
Neurobiol 156:331–339
25. Desmedt JE, Godaux E (1977) Ballistic contractions in man:
characteristic recruitment pattern of single motor units in the
tibialis anterior muscle. J. Physiol 264:673–693
26. Bigland B, Lippold OCJ (1954) The relation between force,
velocity and integrated electrical activity in human muscles. J
Physiol (Lond) 123:214–224
27. Fontana GA (2003) Motor mechanisms and the mechanics of
cough. In: Chung F, Widdicombe J, Boushey H (eds) Cough:
Causes, Mechanisms and Therapy. Oxford: Blackwell Publishing,
pp 193–205