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Cough is a wide field that has been reviewed extensively Morris et al. (1979) found that the two lateral high-
(McCool & Leith 1987, Bouros et al. 1995, Irwin et al. and low-level diameters of the rib cage moved in opposite
1998). The existing descriptions and insights into basic directions during voluntary cough in seven normal
mechanisms of forced expiration and cough are reason- subjects, with this paradoxical movement potentially
ably satisfactory, but knowledge of thoracoabdominal being the mechanism of cough fracture (Pearson 1957).
kinematics involved in cough is still rudimentary. However, because the CW is likely to move with
Increased information on the kinematics of the chest wall more than two degrees of freedom during cough, when
(CW) would allow us to define the relative deflationary the xiphopubic axis shortens (McCool 1995), magne-
contribution of its compartments during fits of coughing. tometers turn out to be inaccurate for partitioning CW
Studies about CW mechanics during cough are scarce and volumes (Vcw) into the contribution of rib cage and
carried out using linearized magnetometers which are abdomen. Studying fits of coughing by optoelectronic
unreliable in conditions other than quiet breathing (QB). plethysmography (OEP) in healthy subjects allows the
Melissinos et al. (1978) reported that paradoxically the non-invasive assessment of Vcw during breathing with-
abdominal diameter increases during decompression out any assumption of the number of degrees of
while the rib cage diameter continuously decreases. freedom of the CW (Cala et al. 1996).
Healthy subjects at rest breathe within the parameters pulmonary function techniques. The study was ap-
of their relaxation characteristics both for the CW as a proved by the institutional Ethics Committee, and
whole and for the rib cage in particular. Crawford et al. informed consent was obtained from each subject.
(1983) and McCool et al. (1985) stated that the nearly
unitary behaviour of the rib cage during breathing must
Protocol
require coordinated muscle activity ‘and that the
intrinsic stability of the rib cage, which presumably We evaluated voluntary single (s) and prolonged (p)
varies substantially between individuals is not adequate coughing performed at functional residual capacity
to account for it’ (McCool et al. 1985). (FRC), and after a maximal inspiration (Max). The
The three-compartment model of the CW (the subjects performed each of the four coughing man-
pulmonary rib cage, abdominal rib cage and abdomen) oeuvres: Cough FRCp, Cough FRCs, Cough Maxp,
(Kenyon et al. 1997) dictates that contraction of the Cough Maxs in a sitting position at least three times. We
abdominal muscles has both a deflationary action on the chose the manoeuvre with the largest peak expiratory
lower rib cage via their insertional component (the flow for analysis.
rectus and obliquus muscles), and an inflationary action
via their non-insertional components (the tranversus
Pulmonary function tests
muscle), the net effect being such that upper rib cage
deflation is commensurate with lower rib cage deflation Routine spirometry, obtained with subjects seated in a
(Kenyon et al. 1997). However, if forces applied to the comfortable armchair, was measured according to
upper rib cage are out of proportion with those applied European Community for Coal and Steel guidelines
to the lower rib cage, distortion might ensue during fits (Quanjer et al. 1993). Lung volumes (FRC, vital capa-
of coughing. In this way the abdominal rib cage is city and total lung capacity) were measured with a body
exposed to greater positive abdominal pressure (Pab) at plethysmograph (Autobox DL 6200; SensorMedics,
the end of expiration during cough (Man et al. 2003). Yorba Linda, CA, USA). The normal values for lung
We therefore hypothesized that uneven distribution of function were those of the European Community for
operating forces may result in rib cage distortion during Coal and Steel (Quanjer et al. 1993).
coughing.
Optoelectronic measurements
Materials and methods
The OEP allows accurate three-dimensional computa-
tion of the Vcw based on coordinates from 89 surface
Subjects
markers attached to the CW surface (Cala et al. 1996).
We evaluated 12 (five women) non-smoking healthy Details of this technique have been thoroughly des-
subjects (mean age 36.3 8.5 years), with normal lung cribed previously (Lanini et al. 2003, Binazzi et al.
function (see Table 1). All were familiar with 2006, Romagnoli et al. 2006). In brief, the coordinates
Age (years) Sex (F/M) BMI (kg m)2) FEV1 (% pv) FEV1/VC (%) FRC (% pv) TLC (% pv) VC (% pv)
BMI: Body Mass Index; FEV1, forced expiratory volume in the first second; FRC, functional residual capacity; TLC, total lung
capacity; VC, vital capacity; pv, predicted value; SD, standard deviation.
3 3
End expiratory volume
2 2 End inspiratory volume
1 1
Vrc, p (l)
Vcw (l)
0 0
–1 –1
–2 –2
–3 –3
QB
Cough FRCs
Cough FRCp
Cough Maxs
Cough Maxp
QB
Cough FRCs
Cough FRCp
Cough Maxs
Cough Maxp
3 3
2 2
1 1
Vrc, a (l)
Vab (l)
0 0
–1 –1
–2 –2
–3 –3
QB
Cough FRCs
Cough FRCp
Cough Maxs
Cough Maxp
QB
Cough FRCs
Cough FRCp
Cough Maxs
Cough Maxp
Figure 1 Chest wall kinematics during cough. Vcw: volume of the chest wall; Vrc,p: volume of pulmonary apposed rib cage; Vrc,a:
volume of abdomen apposed rib cage; Vab: volume of abdomen; QB: quiet breathing; Cough FRCs: a single fit of cough at
functional residual capacity; Cough FRCp: prolonged cough at functional residual capacity; Cough Maxs: a single fit of cough after
Max; Cough Maxp: prolonged cough after Max. Values are mean and SE.
does not apply to different conditions, such as use mouthpieces, nose clip or face masks, which may
respiratory effort during cough, laughing, hyperventila- alter the movements of the mouth and cheeks and the
tion whatever obtained. In addition, particularly in a respiratory system response (Weissman et al. 1984,
clinical setting, adequate calibration data may be McCool et al. 1986). OEP allowed Aliverti et al. (1997)
difficult to obtain because of poor subject cooperation. and Kenyon et al. (1997) to recently revise the mech-
It has also been shown that the CW moves with more anism underlying rib cage distortion in healthy humans.
than two degrees of freedom even during breathing at The two rib cage compartments are mechanically
rest (Ward et al. 1992) and indeed the rib cage has been coupled to each other (Ward et al. 1992) with the
recently described as a two-compartment system: the rib relationship between volume of pulmonary rib cage
cage apposed to the lung (pulmonary rib cage, RCp) (Vrc,p) and volume of abdominal rib cage (Vrc,a)
and the rib cage apposed to the abdomen (RCa) (Ward defining the undistorted rib cage configuration during
et al. 1992, Kenyon et al. 1997). OEP has been recently QB (Kenyon et al. 1997). Accordingly, we evaluated rib
developed that allows the non-invasive assessment of cage distortion during cough as the displacement of
Vcw during breathing without any assumption of the Vrc,p/Vrc,a line away from the relaxed rib cage
number of degrees of freedom of the CW (Cala et al. configuration during QB.
1996). The choice of the OEP system in this study was
based on two fundamental principles: firstly, to safe-
Comments on results
guard the naturalness of cough and secondly, to
guarantee the highest accuracy in measuring lung As shown, Vab and Vrc contribute to deflating CW with
volumes. The lack of interference of the system with cough at FRC and prolonged maximum cough; in
natural breathing is as a result of the fact that it does not contrast, Vrc did not contribute to deflating the Vcw
13.6 6.2
V rc,p (l)
Vrc,p (l)
Vrc,p (l)
10.6 11.3
10.4 11.2 8.65
Vrc,p (l)
11.1 8.60
Vrc,p (l)
10.2
Vrc,p (l)
11.0 8.55
10.0
8.50
9.8 10.9
8.45
9.6 10.8 n7
n6 8.40 n8
9.4 10.7 8.35
2.70 2.75 2.80 2.85 2.90 2.95 3.00 2.12 2.14 2.16 2.18 2.20 2.22 2.24 2.26 2.28 2.18 2.20 2.22 2.24 2.26 2.28 2.30 2.32
Vrc,a (l) Vrc,a (l) Vrc,a (l)
Vrc,p (l)
Vrc,p (l)
Vrc,p (l)
Figure 3 Rib cage distortion during single and prolonged fits of cough after maximal inspiration. Vrc,p: volume of pulmonary
apposed rib cage; Vrc,a: volume of abdomen apposed rib cage; dotted loop: quiet breathing; continuous line: Cough Maxs; dashed
line: Cough Maxp.
Figure 4 Plots of gastric pressure (Pga) vs. esophageal pressure (Pes). The thick identity line is zero Pdi isopleth; continuous and
dashed lines define Pdi over tidal volume during Cough Maxs and Cough Maxp, respectively in subjects 6, 7, 9, 11. Pdi is the trans-
diaphragmatic pressure. For explanation see text.
(transversus muscle) of Pab was not counterbalanced Melissinos et al. (1978), because of the different tech-
by deflating action of insertional muscle component niques. However, it is likely that we found smaller
(external and internal obliquus and rectus muscles) of distortion because we measured volume distortion,
Pab. whereas Morris et al. (1979) and Melissinos et al.
Melissinos et al. (1978) reported that the abdominal (1978) measured rib cage dimension, a circumstance
diameter increased while the rib cage diameter continu- under which deducing volume from a single dimension
ously decreased during decompression. In a preliminary would lead to a systematic overestimation of the volume
report Morris et al. (1979) studied the CW configur- of the rib cage apposed to the abdomen (Kenyon et al.
ation during voluntary cough in seven normal subjects. 1997).
By using linearized magnetometers, they monitored Unitary behaviour of the rib cage requires that the net
antero-posterior diameter of both rib cage (RCa-p) and pressures acting on the two rib cage compartments be
abdomen (Abda-p), and lateral diameters of the rib cage equal, and this would require considerable coordination
at high (RCH-L) and low (RCL-L) levels. CW diameters of the respiratory muscles, the diaphragm, rib cage and
decreased abruptly during the compression phase, abdominal muscles (Crawford et al. 1983, McCool
except for RCa-p. With the glottis opened, RCa-p and et al. 1985, Aliverti et al. 1997, Kenyon et al. 1997).
RCH-L showed a rapid inward motion while RCL-L and The net pressure acting on rib cage compartments must
Abda-p either held their positions constant, or more therefore be closely similar. Inasmuch as the abdominal
commonly moved outwards in paradoxical function. As rib cage is exposed to a large positive inflating Pab at EE
a consequence, the two lateral diameters of the rib cage during cough (Man et al. 2003), this must be counter-
moved in opposite directions during cough. We are balanced by a strong deflating expiratory action result-
aware of the difficulty of comparing the present results ing from active contraction of the expiratory muscles.
with the preliminary data of Morris et al. (1979) and Because the insertional component of the abdominal
Morris, A.J.R., Siafakas, N. & Green, M. 1979. Thor- Romagnoli, I., Gorini, M., Gigliotti, F., Bianchi, R., Lanini, B.,
acoabdominal motion and pressures during coughing Grazzini, M. et al. 2006. Chest wall kinematics, respiratory
(abstract). Thorax 34, 421. muscles action and dyspnoea during arm vs. leg exercise in
Pearson, J.E.G. 1957. Cough fracture of the ribs. Br J Tuberc humans. Acta Physiol (Oxf) 188, 233–246.
Dis Chest 51, 251–254. Ward, M.E., Ward, J.W. & Macklem, P.T. 1992. Analysis of
Quanjer, P.H., Tammeling, G.J., Cotes, J.E. et al. 1993. Lung human chest wall motion using a two-compartment rib cage
volumes and forced ventilatory flows. Report Working Party model. J Appl Physiol 72, 1338–1347.
Standardization of lung function tests, European Commu- Weissman, C., Askanazi, J., Milic-Emili, J. & Kinney, J.M.
nity for Steel and Coal. Official Statement of the European 1984. Effect of respiratory apparatus on respiration. J Appl
Respiratory Society. Eur Respir J 6 (Suppl. 16), 5–40. Physiol 57, 475–480.