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Acta Physiol 2007, 190, 351–358

Chest wall kinematics during cough in healthy subjects

B. Lanini,1 R. Bianchi,1 B. Binazzi,1 I. Romagnoli,1 F. Pala,1 F. Gigliotti1 and G. Scano1,2


1 Section of Respiratory Rehabilitation, Fondazione Don C. Gnocchi ONLUS (IRCCS), Pozzolatico, Firenze, Italy
2 Section of Respiratory Disease, Department of Internal Medicine, University of Florence, Firenze, Italy

Received 30 October 2006, Abstract


revision requested 11 December Aim: The study of kinematics of the chest wall (CW) could allow us to define
2006,
the relative deflationary contribution of its compartments during fits of
revision received 1 February 2007,
accepted 8 February 2007 coughing. We hypothesized that if forces applied to the lung apposed rib cage
Correspondence: B. Lanini, MD, are not commensurate with those applied to the abdomen-apposed rib cage,
Section of Respiratory cough could result in rib cage distortion.
Rehabilitation, Fondazione Don C. Methods: In 12 (five women) healthy subjects we evaluated the volumes of
Gnocchi ONLUS (IRCCS), Via
CW (Vcw) and its compartments: the lung apposed rib cage, the abdomen
Imprunetana124, 50020
Pozzolatico, Firenze, Italy.
apposed rib cage and the abdomen, by optoelectronic plethysmography. The
E-mail: laninibarbara@yahoo.it loop of volume of the lung apposed rib cage/volume of the abdomen apposed
rib cage allowed the calculation of mean rib cage distortion, resulting in a
dimensionless number which, when multiplied by 100, gives percentage
distortion. Each subject performed voluntary single and prolonged coughing
efforts at functional residual capacity (FRC) and after maximal inspiration
(max). The normal level of mean distortion was set at <0.5%.
Results: The three compartments contributed to reducing end-expiratory
Vcw during cough at FRC and prolonged maximum cough, with the latter
resulting in the greatest CW deflation. Mean rib cage distortion did not differ
between men and women (P > 0.1), but tended to significantly increase from
single to prolonged Cough Max (1.3%  1.0 vs. 2.3%  1.6, respectively;
P ¼ 0.06).
Conclusion: Rib cage distortion may ensue during coughing, probably as a
result of uneven distribution of forces applied to the rib cage.
Keywords chest wall kinematics, cough, rib cage distortion.

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).

Ó 2007 The Authors


Journal compilation Ó 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01701.x 351
Chest wall and cough Æ B Lanini et al. Acta Physiol 2007, 190, 351–358

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

Table 1 Anthropometric and respiratory functional data of the subjects

Age (years) Sex (F/M) BMI (kg m)2) FEV1 (% pv) FEV1/VC (%) FRC (% pv) TLC (% pv) VC (% pv)

1 29 F 23.4 104 74 91 103 108


2 30 M 27.8 98 98 106 112 106
3 54 M 23.1 85 85 101 84 80
4 40 F 22.1 88 88 98 97 96
5 34 F 26.3 105 82 109 113 97
6 38 F 22.8 95 77 92 101 98
7 33 M 26.0 89 90 102 98 107
8 31 F 20.4 93 79 112 103 95
9 28 M 22.7 97 84 93 117 103
10 50 M 18.1 103 92 81 93 97
11 40 M 20.4 108 89 97 109 106
12 29 M 20.7 107 91 105 115 110
Mean 36.3 22.1 100.8 85.6 98.9 103.7 104.6
SD 8.5 3.0 11.6 5.5 8.8 9.9 12.6

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.

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352 Journal compilation Ó 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01701.x
Acta Physiol 2007, 190, 351–358 B Lanini et al. Æ Chest wall and cough
of the markers were tracked by four infrared charge- with the plot being a vertical line). Some subjects with
coupled TV-cameras (two 4 m in front and two 4 m minimal (no. 2) or null (no. 6, 8) distortion during
behind the subject) at a sampling rate of 50 Hz. Cough Maxs exhibited an increased distortion during
Volumes were calculated from the surface triangulation Cough Maxp (Table 2). Group mean level of distortion
between the marker points. The total Vcw was modeled tended to be greater (P ¼ 0.06) during Cough Maxp
as the sum of volume of the rib cage apposed to the lung (2.3  1.6%; range 1  0.5%) than during Cough
(Vrc,p), volume of the rib cage apposed to the abdomen Maxs (1.3  1.0%; range 0.9  0.6%), with maximal
(Vrc,a) and volume of the abdomen (Vab) (see Fig. 4 in distortion being approx. 5% in subject no. 12 during
Kenyon et al. 1997). Cough Maxp (Table 2). Nonetheless, distortion did not
differ during Cough Maxs and Cough Maxp in men
(1.2  0.5% and 2.4  0.1%, respectively, P ¼ ns) just
Rib cage distortion measurements
as in women (1.6  1.6% and 2.1  0.9%, respect-
The undistorted rib cage configuration was defined by ively, P ¼ ns), with no gender difference (P ¼ ns).
plotting the Vrc,p loop against the Vrc,a loop during Individual cough lines are plotted on undistorted loops
tidal volume (VT) breathing. Rib cage distortion was in Figure 3. Cough lines were shifted down and to the
evaluated comparing the Vrc,p–Vrc,a plots to the right, indicating for a given Vrc,a a lower than relaxed
undistorted rib cage configuration in the volume range Vrc,p in subjects no. 1, 3, 6, 7, 11 (in part) and 12
of tidal breathing during Cough Maxp and Cough during Cough Maxs and in subjects no. 1, 5–7 and 8 (in
Maxs. We used the method of Chihara et al. (1996) and part) during Cough Maxp. Cough lines were shifted
measured the perpendicular distance of the cough upward and leftward in subjects no. 2, 5, 8–10 and 11
configuration away from the relaxation line divided by (in part) during Cough Maxs and in subjects no. 2, 3,
the value of Vrc,p at the insertion point. This results in a 9–12 during Cough Maxp. Subjects no. 3, 5, 12 changed
dimensionless number which, when multiplied by 100, the pattern of distortion from single to prolonged
gives percentage distortion. The method allows assess- cough.
ment of inter-individual rib cage distortion. Based on
the data of Kenyon et al. (1997), the mean acceptable
Discussion
rib cage distortion was arbitrarily set at <0.5%.
The novel findings in this study are as follows: (i) the
three compartments contribute to reducing end-expir-
Statistical analysis
atory Vcw during cough at FRC, prolonged maximum
Data are presented as mean  SD. Differences between cough and with the exception of the rib cage, during
values were tested by Student’s paired t-test. The Vcw single maximum cough; (ii) prolonged fits of maximum
compartments during cough manoeuvres were com- cough result in the greatest CW deflation; and (iii)
pared using two-way analysis of variance (anova). The mild to moderate levels of rib cage distortion were
Bonferroni test was used for multiple comparisons. found during both single and prolonged maximum
P < 0.05 was considered to be statistically significant. cough, with the difference being close to a significant
All statistical procedures were carried out using the level (P ¼ 0.06). Had we studied more subjects the
Statgraphics Plus 5.1 statistical package (Statistical difference would have reached statistical significance
Graphics Corp., Rockville, MD, USA). (P < 0.05).

Results Comments on methodology


Figure 1 shows the changes in the compartmental Vcw Previous studies on the effect of coughing on thoraco-
during QB and the four cough manoeuvres (Cough abdominal mechanics were carried out using magne-
FRCs, Cough FRCp, Cough Maxs, Cough Maxp). tometers (Melissinos et al. 1978, Morris et al. 1979).
Compared with QB, the Vcw compartments during all This non-invasive method considered the overall VT as
cough manoeuvres, but not the Vrc during Cough Maxs, the sum of the concurrent changes in volume of the rib
contributed to reducing end-expiratory volume dis- cage (VTrc) and abdomen (VTab) (Konno & Mead
placement of the CW (anova, P < 0.01); this is shown 1967). Within limits, these two compartments can be
in Figure 2 where the plots of Vrc/Vab at end-expiration considered has having a single degree of freedom, so
(EE) are all below the identity line during Cough Maxs. that when appropriately calibrated, the summed motion
Rib cage distortion means and ranges were assessed of the two parts yields VT. However, the validity of the
by plotting Vrc,p vs. Vrc,a during Cough Maxs and experimental calibration coefficients used to convert
Cough Maxp in all subjects but one (subject no. 4, in one or two dimensions to volume is limited to the
whom no change in Vab was found when she relaxed, conditions under which the calibration is performed and

Ó 2007 The Authors


Journal compilation Ó 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01701.x 353
Chest wall and cough Æ B Lanini et al. Acta Physiol 2007, 190, 351–358

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

Ó 2007 The Authors


354 Journal compilation Ó 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01701.x
Acta Physiol 2007, 190, 351–358 B Lanini et al. Æ Chest wall and cough
Table 2 Rib cage distortion

Subject no. Cough Maxs (%) Cough Maxp (%)

1 3.67 (2.9–4.3) 3.45 (2.7–4.1)


2 0.69 (0.6–0.8) 3.21 (2.7–3.9)
3 1.88 (1.2–2.5) 2.40 (1.0–2.8)
5 1.85 (0.5–2.9) 1.96 (1.4–2.6)
6 0.33 (0.3–0.4) 1.39 (1.3–1.4)
7 1.38 (0.5–1.8) 0.43 (0.2–0.6)
8 0.38 (0.1–0.5) 1.54 (0.6–2.2)
9 0.75 (0.3–1.2) 0.40 (0.2–0.5)
10 1.89 (1.5–2.3) 4.49 (3.8–5.1)
11 0.97 (0.4–1.7) 1.30 (0.7–2.0)
12 0.86 (0.7–1.1) 5.03 (4.8–5.3)
Mean 1.3 2.3
SD 1.0 1.6
P value 0.06

Each value is the mean of three measurements and ranges in


parenthesis.
Cough Maxs, single fit of coughing after maximal inspiration;
Figure 2 Plot of changes (D) in end expiratory volume of Vrc
Cough Maxp, prolonged cough after maximal inspiration.
and Vab during Cough Maxs. VrcEE: end expiratory volume of
rib cage; VabEE: end expiratory volume of abdomen. Dotted
line is identity line.

action of the diaphragm and other inspiratory muscles


with a single maximum cough. Possible reasons might (Coryllos 1937, Melissinos et al. 1978, Morris et al.
involve either or both of the following: (i) relatively 1979, Melissinos et al. 1981, Bouros et al. 1995,
small pressure production of expiratory rib cage mus- Kyroussis et al. 1996); (ii) inflating action operating
cles during expulsive phase because of antagonistic on the rib cage by non-insertional muscular component

7.5 13.8 13.8 6.4


7.4 13.7 13.7 6.3
7.3 13.6
Vrc,p (l)

13.6 6.2
V rc,p (l)

Vrc,p (l)
Vrc,p (l)

7.2 13.5 6.1


7.1 13.5 13.4
7.0 6.0
13.4 13.3
6.9 13.2 5.9
6.8 n1 13.3 n2 13.1 n3 5.8 n5
6.7 13.2 13.0 5.7
1.85 1.90 1.95 2.00 2.05 2.10 3.35 3.40 3.45 3.50 3.55 2.70 2.75 2.80 2.85 2.90 2.95 3.00 1.76 1.78 1.80 1.82 1.84 1.86 1.88 1.90 1.92 1.94 1.96
Vrc,a (l) Vrc,a (l) Vrc,a (l) Vrc,a (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)

12.6 11.1 15.4


12.5 10.7 11.0 15.2
12.4 10.7 10.9 15.0
Vrc,p (l)

Vrc,p (l)
Vrc,p (l)

Vrc,p (l)

12.3 10.6 14.8


10.8
10.6 14.6
12.2 10.7
10.5 14.4
12.1 10.5 10.6 14.2
12.0 n9 10.4 n 10 10.5 14.0 n 12
n 11
11.9 10.4 10.4 13.8
3.64 3.66 3.68 3.70 3.72 3.74 3.76 3.78 3.80 2.65 2.70 2.75 2.80 2.85 2.90 3.1 3.2 3.3 3.4 3.5 3.55 3.60 3.65 3.70 3.75 3.80 3.85 3.90
Vrc,a (l) Vrc,a (l) Vrc,a (l) Vrc,a (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.

Ó 2007 The Authors


Journal compilation Ó 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01701.x 355
Chest wall and cough Æ B Lanini et al. Acta Physiol 2007, 190, 351–358

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

Ó 2007 The Authors


356 Journal compilation Ó 2007 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2007.01701.x
Acta Physiol 2007, 190, 351–358 B Lanini et al. Æ Chest wall and cough
muscles is a major contributor to this expiratory action References
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