Vol. 90, Issue 4, 1441-1446, April 2001
Respiratory dynamics during laughter
Mario
Filippelli1,
Riccardo
Pellegrino2,
Iacopo
Iandelli1,
Gianni
Misuri1,
Joseph R.
Rodarte3,
Roberto
Duranti5,
Vito
Brusasco4, and
Giorgio
Scano1,5
1 Fondazione Don C. Gnocchi "ONLUS," UOF di
Riabilitazione Respiratoria, Centro di S. Maria agli Ulivi, 50020 Pozzolatico, Firenze, Italy; 2 Fisiopatologia Respiratoria,
Azienda Ospedaliera S. Croce e Carle, 12100 Cuneo, Italy;
3 Respiratory Section, Baylor College of Medicine, Houston,
Texas 77030; 4 Cattedra di Fisiopatologia Respiratoria, DISM,
Università di Genova, 16132 Genoa, Italy; and 5 Section of
Immunoallergology and Respiratory Disease, Department of Internal
Medicine, University of Florence, 50134 Firenze, Italy
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ABSTRACT |
Lung and chest wall
mechanics were studied during fits of laughter in 11 normal subjects.
Laughing was naturally induced by showing clips of the funniest scenes
from a movie by Roberto Benigni. Chest wall volume was measured by
using a three-dimensional optoelectronic plethysmography and was
partitioned into upper thorax, lower thorax, and abdominal
compartments. Esophageal (Pes) and gastric (Pga) pressures were
measured in seven subjects. All fits of laughter were characterized by
a sudden occurrence of repetitive expiratory efforts at an average
frequency of 4.6 ± 1.1 Hz, which led to a final drop in
functional residual capacity (FRC) by 1.55 ± 0.40 liter
(P < 0.001). All compartments similarly contributed to
the decrease of lung volumes. The average duration of the fits of laughter was 3.7 ± 2.2 s. Most of the events were associated
with sudden increase in Pes well beyond the critical pressure necessary to generate maximum expiratory flow at a given lung volume. Pga increased more than Pes at the end of the expiratory efforts by an
average of 27 ± 7 cmH2O. Transdiaphragmatic pressure
(Pdi) at FRC and at 10% and 20% control forced vital capacity below FRC was significantly higher than Pdi at the same absolute lung volumes
during a relaxed maneuver at rest (P < 0.001). We
conclude that fits of laughter consistently lead to sudden and
substantial decrease in lung volume in all respiratory compartments and
remarkable dynamic compression of the airways. Further mechanical
stress would have applied to all the organs located in the thoracic
cavity if the diaphragm had not actively prevented part of the increase in abdominal pressure from being transmitted to the chest wall cavity.
respiratory muscles; chest wall kinematics; expiratory flow
limitation; laughing
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INTRODUCTION |
LAUGHING IS A NATURAL
MANEUVER triggered by emotion. During laughter, stress is applied
to the chest wall, causing rapid and substantial motion (4, 6,
7). Detailed descriptions of respiratory system dynamics have
not been published so far because of the inability to measure chest
wall compartmental volumes and motion without instrumentation that
affects them. A detailed knowledge of the dynamic events occurring in
the respiratory system during episodes of laughter may help understand
the pattern and magnitude of physiological reaction of the chest wall
to such a forceful mechanical event.
The present paper reports on the application of noninvasive
optoelectronic plethysmography (OEP) (1, 3) to assess
breathing movements during fits of laughter in 11 normal subjects. The
OEP is capable of computing the changes of absolute lung volumes of the
entire chest wall by monitoring the three-dimensional movements of
markers placed on the chest and abdominal walls (1, 3).
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METHODS |
Subjects.
We studied 11 normal individuals whose anthropometric and functional
respiratory characteristics are presented in Table
1. All were very familiar with pulmonary
function techniques. Four of the individuals were current smokers. The
study was approved by the institutional Ethics Committee, and informed
consent was obtained from each subject.
Standard spirometry and lung volume measurements.
Forced vital capacity (FVC) and forced expiratory volume expired in
1 s were measured by a water-sealed spirometer (Pulmonet III,
SensorMedics, Yorba Linda, CA). Functional residual capacity (FRC) was
measured by helium-dilution rebreathing technique. Residual volume (RV)
was computed by subtracting expiratory reserve volume from FRC,
and total lung capacity (TLC) was computed by adding vital
capacity to RV. All the tests were done according to the standards
recommended by the American Thoracic Society (2).
Lung mechanics.
Flow at the mouth was measured through a no. 3 Fleisch pneumotachograph
connected to a pressure transducer (±2 cmH2O, Validyne, Northridge, CA). Volume was electrically integrated from the flow signal. Esophageal (Pes) and gastric pressures (Pga) were measured by
two 10-cm-long thin balloons positioned in the lower one-third of the
esophagus and into the stomach, respectively. Each balloon was
connected to a differential pressure transducer (±100
cmH2O, Validyne, Northridge, CA) through a thin catheter.
The frequency response of the balloon-catheter systems was adequate up
to >8 Hz, and accuracy was >99% up to 200 cmH2O with the
balloon filled with 1-1.5 ml of air. The esophageal balloon was
filled with 1 ml of air and the gastric balloon with 1.5 ml of air.
Mouth pressure (Pao) was recorded by a third Validyne pressure
transducer (±100 cmH2O). Placement of the esophageal
balloon was considered correct if the difference between Pes and Pao
remained substantially unchanged with the subjects making gentle
efforts against a closed shutter. Transdiaphragmatic pressure (Pdi) was
the difference between Pga and Pes. Flow, volume, Pes, Pga, Pdi, and
Pao signals were synchronized to the kinematic signals of the OEP and
sent to an IBM-compatible personal computer through an RTI 800 analog-to-digital card for subsequent analysis.
Compartmental volume measurements.
Kinematic analysis of the chest wall was computed by using the OEP
system. Details of the technique are reported elsewhere (1,
3). In brief, four cameras, two 4 m in the front and two
4 m behind the subject, tracked the three-dimensional movements of
89 small surface markers attached to the skin of the trunk with
double-sided adhesive tape. The markers, 5-mm hemispheres coated with
reflective paper, were positioned according to Cala et al.
(3) along seven horizontal and vertical lines both
anteriorly and posteriorly to the chest wall and abdomen. Their
movements were tracked by the cameras that lit them through infrared
light-emitting diodes coaxial with the lenses. According to Cala et
al., the positioning of the markers allows not only computation of the entire volume of the chest and abdomen beneath the markers with great
accuracy but also its partitioning into three respiratory functional
compartments: pulmonary rib cage (Vrc,p), abdominal rib cage (Vrc,a) or
appositional area, and abdominal compartment (Vab). All
maneuvers were recorded at a sampling frequency of 100 Hz.
Study protocol.
Standard spirometry and absolute lung volume measurements were obtained
before the study.
Each study day consisted of the following measurements. First,
partial and maximal forced expiratory maneuvers were done by asking the
subjects to blow out as fast as they could from the end of tidal
inspiration (partial maneuver) and from TLC immediately after taking a
deep breath (maximal maneuver). The maneuvers were done until three
reproducible curves were obtained. Second, esophageal and gastric
balloons were positioned in seven individuals after topical anesthesia
of nose and throat. The latter was carefully done to minimize any
discomfort due to the catheters in the throat and interference with
breathing pattern adopted by the subjects. In some cases, anesthesia of
the throat was repeated during the study if requested by the subjects.
Then, isovolume pressure-flow curves were recorded according to the
method of Olafsson and Hyatt (9). Briefly, the subjects
were asked to perform four to six expirations from TLC to RV with
graded and fairly constant efforts. The lowest esophageal pressure
associated with maximum flow at a given lung volume was defined as
critical pressure (Pcrit) and estimated on plots of flow and esophageal
pressure against chest wall volume (Vcw). Pcrit was taken at
the volume at which Pes showed a sudden increase and flow tended to
decrease. The series of expiratory maneuvers allowed us to calculate
Pcrit over the tidal breathing range and ~1 liter below as shown by
the oblique line in Fig. 1. Third,
subjects were instructed to breathe quietly without the mouthpiece and
pneumotachograph and not to think about their breathing. Once they
seemed at their ease, two sets of 3-min tidal breathing were recorded
solely with the OEP system. Finally, the subjects were asked to
watch three clips of the funniest scenes of the movie "Berlinguer ti
voglio bene" by Roberto Benigni. All subjects had spontaneous
episodes of laughter.
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Fig. 1.
Esophageal pressure (Pes) plotted against total chest wall volume
(Vcw) in 3 individuals during a fit of laughter. Oblique line is
critical pressure (Pcrit), i.e., the pressure at which maximum flow is
achieved. Beginning of laughter is marked by an arrow. Left:
Pes swings are constantly greater than Pcrit, thus suggesting
occurrence of expiratory airflow limitation during the fit.
Center: expiratory effort is of less magnitude, and Pes
swings only in part exceed Pcrit. Right: decrease in lung
volume is associated with poor expiratory effort, so that Pes swings
remain below Pcrit. Under this condition, expiratory airflow limitation
is never attained.
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Statistical analysis.
Data are presented as means ± SD. Differences between values were
tested by Student's paired t-test. The time constant of the
change in Vcw, Vrc,p, Vrc,a, and Vab occurring over time during the
laughter was measured by exponentially regressing the raw data and
calculating the time at which the decrease in volume was 63.2% of the
entire change. P < 0.05 was considered to be statistically significant.
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RESULTS |
Resting conditions.
Pulmonary function was within the normal range in all subjects (Table
1). Breathing pattern at rest as recorded by the OEP system was
accomplished with a tidal volume (VT) of 0.58 ± 0.13 liter (11 ± 3% of vital capacity) and a frequency of 15 ± 5. Vab, Vrc,a, and Vrc,p contributed 51.4 ± 14.6%, 12.7 ± 5.5%, and 35.9 ± 11.5% of VT, respectively. FRC was
on average 3.6 ± 0.4 liter below TLC, which is ~52% of TLC
predicted. During quiet breathing, Pes varied from 
6.5 ± 1.5 cmH2O at FRC to 9.0 ± 2.6 cmH2O at end-inspiration. Pga was 8.2 ± 3.1 cmH2O and
12.1 ± 2.7 cmH2O at the same volumes. Average Pcrit
at FRC was 14.0 ± 3.5 cmH2O. Pdi at FRC and at 10%
and 20% control FVC below FRC recorded during the slowest maximal
expiratory maneuver was 14.4 ± 4.7, 17.2 ± 4.7, and
20.6 ± 4.0 cmH2O, respectively.
During laughter.
Watching the clips of the movie triggered fits of laughter in every
subject. For simplicity, only the first two fits were used in the
statistical analysis. The fits excluded from the study were strikingly
similar to the first two.
Laughter was characterized by small and consecutive expiratory efforts
starting within the VT at an average frequency of 4.6 ± 1.1 Hz, which caused a systematic and consistent decrease in lung
volume to 1.55 ± 0.40 liter below FRC. The time constant of
decrement in lung volume was 0.8 ± 0.5 s (Table
2), and average duration of the laughter
was 3.7 ± 2.2 s. Pes and Pga from two representative
subjects are shown in Figs. 2 and
3.
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Fig. 2.
Recording of optoelectronic plethysmographic (OEP) signals (Vrc,p,
upper thorax; Vrc,a, lower thorax; Vab, abdomen) and Pes and gastric
pressures (Pga) during tidal breathing and a fit of laughter in a
representative subject (subject 9). At the beginning of
laughter (arrow), the volume of all compartments suddenly
decreased to reach a minimum value within ~1 s. This was associated
with occurrence of short and consecutive expiratory efforts briefly
interrupted by inspiratory efforts, as demonstrated by swings in Pga
and Pes. The entire fit lasted ~5 s, and then regular breathing was
resumed in a couple of breaths.
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Fig. 3.
Recording of OEP and pressures signals in another individual
(subject 2). In this case, the fit occured with less
intensity than in the subject of Fig. 2, as evidenced by a slower
decrease in lung volume over time. Arrow marks beginning of laughter.
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All three chest wall compartments contributed similarly to the decrease
in FRC either in terms of volumes or time constants (Table 2).
Laughter was nearly always associated with sudden increase in Pes of
various intensity, in general well beyond Pcrit necessary to generate
maximum expiratory flow at a given lung volume, thus suggesting
occurrence of expiratory flow limitation. In two of the seven subjects
who had the esophageal and gastric balloons in place, Pes did not
exceed Pcrit on both series of laughter, even though there was a
substantial reduction of lung volume. Figure 1 illustrates the range of
responses observed. The increase on Pga was systematically greater than
Pes by an average of 27 ± 7 cmH2O over the entire
time of the fit (Figs. 2 and 3). Pdi measured at the end of the brief
expiratory efforts at FRC and at 10% and 20% control FVC below FRC
was significantly higher than Pdi at the same absolute lung volumes
measured during a slow expiratory maneuver at rest (P < 0.001) (Fig. 4).
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Fig. 4.
Transdiaphragmatic pressure (Pdi) recorded at functional
residual capacity (FRC) and at 10 and 20% of control vital capacity
(FVC) below FRC during a slow maximal expiratory maneuver
( ) and at the end of the expiratory efforts during the
fits of laughter ( ). Vertical bars are SD.
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Time derivatives of Pes (dP/dt) of the single
small expiratory efforts during the first and second fits of laughter
were on average 117 ± 79 and 111 ± 68 cmH2O/s,
respectively (Table 3).
Regular breathing was resumed within two to three breaths after
cessation of the fits by bringing VT, Pes, and Pga back to normal values (Fig. 2).
No significant differences in breathing pattern were seen between the
subjects with and without the esophageal and gastric balloons (Table
4).
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Table 4.
Changes of total chest wall and compartmental volumes at FRC with
and without esophageal and gastric balloons
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DISCUSSION |
Dynamic events occurring in the chest wall during laughing may be
summarized as follows. Episodes of laughter were associated with a
remarkable decrease in lung volume due to sudden and sustained increase
in Pga and Pes. The latter substantially exceeded Pcrit with few
exceptions, thus generating expiratory flow limitation and dynamic
collapse in the airways downstream from the choke point. Higher Pdi at
the end of the consecutive expiratory efforts than during a slow
expiratory maneuver over the same absolute lung volumes suggests that
the diaphragm tended to counteract the excess of pressure generated on
the abdominal site, thus protecting intrathoracic structures from
further mechanical stress and compression.
Comments on methodology.
The choice of the OEP system in this study was based on two fundamental
principles: first, to safeguard the naturalness of the laughter and
second, to guarantee the highest accuracy in measuring lung volumes.
The lack of interference of the system with natural breathing is due to
the fact that it does not use mouthpieces, nose clips, or face masks,
which may alter the movements of the mouth and cheeks and the
respiratory system response. Cala et al. (3) reported that
the system detects changes in volume during tidal and maximal
respiratory maneuvers as accurately as spirometry does, which is more
than adequate for this study. Staying seated in a constrained position
with the arms on armrests was the only minimal trouble for the subject,
but certainly not enough to disturb laughing.
The esophageal and gastric balloons could have disturbed the
naturalness of laughter. To minimize these potential effects, we
selected our subjects from among those who had previously experienced positioning of balloons for other studies with no negative experience and anesthetized the nose and throat with great care. Furthermore, comparison of the data during fits of laughter with those of a subgroup
of four individuals who did not swallow balloons (Table 4) did not
highlight systematic differences, thus making us confident that the
balloons did not reasonably affect the breathing pattern during laughing.
Comments on results.
Decrease in FRC after laughing occurred with a fairly variable time
constant, which was on average <1 s, depending on the intensity of the
laughter. Perhaps, in few extreme cases, fits of laughing might
resemble to a forced expiration. On average, the decrement of FRC was
approximately two-thirds of the expiratory volume reserve, but in no
cases did FRC fall to RV. Interestingly, when the lowest value of FRC
was attained, oscillations of Pes were accompanied by only minute
motions of the chest wall, indicating that there was flow limitation
with near-zero flow, which was independent of pleural pressure. The
changes in lung volumes are inclusive of both exhaled volume and
thoracic gas compression, which cannot be obviously partitioned in the
present study. A rough estimation can, however, be done as follows.
Because of the rhythmic adduction and abduction of the vocal cords
during the laughter (4), the glottis closure at the very
beginning of each expiratory effort would have slowed down expiratory
flow and increased alveolar pressure. The latter was associated with increase in gas compression when pleural pressure exceeded Pcrit. Assuming a maximum time for glottis closure of 0.1 s, an increase in esophageal pressure over time of ~100 cmH2O/s as
estimated from Table 3, and a thoracic gas volume of 4 liters, then
thoracic gas compression volume would amount to 40 ml. In contrast,
under conditions of no expiratory flow limitation [pleural
pressure < Pcrit] the rapid movements of the vocal cords could
have just slightly braked expiration, thus decreasing flow and
modulating the classical sound emitted with laughing. Additional
thoracic gas compression occurs with esophageal pressure exceeding
Pcrit. For a difference between the two pressures of 50 cmH2O and a thoracic gas volume the same as before, the
amount of gas compressed in the chest cavity would be 200 ml.
Therefore, we can fairly estimate that thoracic gas compression volume
accounted for <20% of the entire decrease of the chest wall volume
during laughter.
Assuming that airway caliber changes proportionally to the cube root of
lung volume (11), the decrease in FRC itself during laughing determined a decrease in external airway diameter by ~20% and an increase in airway resistance by six to eight
times, depending on the thickness of the airway wall (8).
Although the fits were never as intense as during a forced expiration, the increase in Pes generally exceeded Pcrit by a variable amount, thus
generating airflow limitation conditions. Only toward the end of the
episode did Pes tend to return toward its control values, unless
another fit of laughter started again. Therefore, decrease in lung
volume during laughing was associated with substantial decrease in
airway caliber and consequent rise in airflow resistance, especially
when the airways underwent dynamic collapse. In these healthy
individuals, however, the unstable mechanical conditions of the airways
during the fit did not last for a long time, because normal Pes, Pga,
and VT were resumed in a couple of tidal breaths. In a few
cases (2 out of 7), the fits of laughter were characterized by a
progressive decrease in FRC with Pes becoming slightly positive but
never exceeding Pcrit (Fig. 1, right). The two patterns
presented in this study reflect the variety of effort applied to the
respiratory system during laughing.
The decrease in FRC was quite uniform across the chest wall, in that
all the compartments decreased size during the fits similarly to each
other. This implies that, although the abdominal muscles contracted and
increased Pga and Pes, the internal intercostal muscles contracted too
and decreased the size of the upper chest wall. In addition, they did
so similarly to the abdominal muscles as the time constant of the
changes in FRC of the Vrc,p was not significantly different from that
of the other compartments. Altogether, these data would suggest that,
when the subjects laugh, all the expiratory muscles are well
coordinated to expel gas out of the chest wall and generate the typical
sounds associated with laughing.
If the expiratory muscles played a leading role in shaping the dynamic
response of the respiratory system during the fits of laughter, the
diaphragm played certainly the critical role to protect the lung and
the other intrathoracic organs from the excess in pressure generated in
the abdominal compartment. This is documented by significantly higher
values of Pdi during laughing than during a slow expiratory maneuver
over the same absolute lung volumes. How this occurred is a matter of
speculation. The activation of the expiratory muscles during the fits
of laughter was not continuous as during a forced expiration but was
interrupted by brief inspiratory efforts as documented by the swings in
Pga and Pes. The duration of the small expiratory efforts was on
average <100 ms, which is too short for the postinspiratory activity
of the diaphragm to disappear. If so, then the diaphragm could not help
remaining active throughout the laughter, thus behaving like an elastic
load capable of contrasting the force generated by the abdominal muscle
contraction. From a teleological point of view, cutting Pga in half
could protect the intrathoracic structures from the dangers of
exaggerated pressure and collapse.
In conclusion, fits of laughter are accompanied by remarkable though
transient disturbance of the chest wall that neither is certainly
harmful nor triggers remote responses in healthy humans. However, this
might not be the case in some individuals in whom laughter causes
sudden cataplexy (7, 10), in others in whom laughing may
be associated with syncope episodes (5), or again in
others in whom laughing may seriously precipitate bronchospasm
(6). The data of the present study may suggest that the
rapid and exaggerated increase in pleural pressure that decreases FRC
and causes expiratory flow limitation even for a few seconds might even
play a remarkable role in the pathogenesis of the above-mentioned
phenomena associated with laughter.
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ACKNOWLEDGEMENTS |
We thank Roberto Benigni, whose movie was not just pleasant to see
but also important for science.
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FOOTNOTES |
This research was supported by grants of Fondazione Don C. Gnocchi
Istituto di Ricovero E Cura a Carattere Scientifico, Pozzolatico, Firenze, and of the University of Florence, Italy.
Address for reprint requests and other correspondence: G. Scano, Section of Immunoallergology and Respiratory Disease, Dept. of
Internal Medicine, Univ. of Florence, viale Morgagni 85, 50134, Firenze, Italy (E-mail: g.scano{at}dfc.unifi.it).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 23 August 2000; accepted in final form 9 November 2000.
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ABSTRACT
INTRODUCTION
