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Department of Pediatrics and Pulmonary Research Unit, Faculty of Medicine, University of Sherbrooke, Sherbrooke, Quebec J1H 5N4, Canada
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Diaz, Véronique, Irenej Kianicka, Patrick
Letourneau, and Jean-Paul Praud. Inferior pharyngeal
constrictor electromyographic activity during permeability pulmonary
edema in lambs. J. Appl. Physiol. 81(4): 1598-1604, 1996.
Newborn mammals exhibit an active expiratory upper airway
closure during the first hours of extrauterine life. We have recently
shown that permeability pulmonary edema led to active expiratory
glottic closure in awake newborn lambs while hypoxia (inspired
O2 fraction 8%; 15 min) did not. In the present
study, we tested the hypothesis that expiratory glottic closure was
accompanied by an increase in pharyngeal constrictor muscle expiratory
electromyographic (EMG) activity. We studied seven awake nonsedated
lambs aged 8-20 days. Airflow (facial mask + pneumotachograph),
blood gases (arterial catheter), and EMG activity of both the
thyroarytenoid muscle (a glottic adductor) and the inferior pharyngeal
constrictor muscle were recorded before and after intravenous injection
of halothane (0.05 ml/kg) to induce a permeability pulmonary edema. A
central apnea (duration 15 s to 5 min) with continuous thyroarytenoid
and inferior pharyngeal constrictor activity was observed within
seconds after halothane injection. One lamb died despite rescuing
maneuvers. An expiratory phasic thyroarytenoid and inferior pharyngeal
constrictor muscle activity with simultaneous zero airflow gradually
took place and, by 30 min after halothane injection, was present at
each expiration in the six remaining lambs. Expiratory glottic and
pharyngeal constrictor muscle EMG activity was subsequently present
during the whole study period (1.5-5 h), even after correction of
the initial hypoxia. Permeability lung edema was present at postmortem examination in all seven lambs. We conclude that a permeability pulmonary edema induced by intravenous halothane in nonsedated lambs
enhances both glottic and pharyngeal constrictor muscle expiratory EMG.
We hypothesize that expiratory contraction of the inferior pharyngeal
constrictor muscle could participate in the active expiratory upper
airway closure; this, in turn, might improve alveolocapillary gas
exchange by increasing the end-expiratory lung volume.
expiratory airflow braking; pharyngeal constrictor
muscle
INTRODUCTION ACTIVE EXPIRATORY AIRFLOW BRAKING is an essential
ventilatory strategy in newborn mammals (19). It can be recorded in
normal-term human neonates in the first minutes after birth, during
initial adaptation to extrauterine lung ventilation (6). In
pathological situations, the expiratory airflow braking becomes audible
as an expiratory grunting. This classic alarm signal was recognized long ago in hyalin membrane disease, transient tachypnea of the newborn, meconium aspiration, and infectious alveolitis. Its importance as a defense mechanism in these situations has been highlighted by the
observation that endotracheal intubation (i.e., bypassing the upper
airways) worsened hypoxia and led to severe acidosis (8).
The mechanisms underlying expiratory grunting are still under debate.
Although it is well accepted that an active glottic closure brought
about by the contraction of glottic adductor muscles (i.e., the
thyroarytenoid muscle) accompanies expiratory airflow braking (12), the
electrical activity [electromyographic (EMG) activity] of
the other upper airway muscles has not been systematically studied in
such situations. Moreover, the factors triggering active expiratory
glottic closure are still unresolved. Hypoxia, usually present in
neonates with respiratory problems, has been considered by some
researchers to be responsible for expiratory grunting (2, 8). However,
in a recent series of experiments conducted in term lambs from the
first day of life, Praud et al. (22, 23, 25) have shown that hypoxia
does not lead to expiratory airflow braking or to enhancement of
thyroarytenoid muscle EMG activity. And from the premise
that all neonates with expiratory grunting have excess water in their
lungs, we have shown that pulmonary edema in lambs consistently
triggered an expiratory thyroarytenoid muscle contraction with airflow
braking (24). These results led us to hypothesize that vagally mediated
afferent activity could be responsible for expiratory grunting in
neonates, in agreement with previous studies in lambs showing that
volume receptive information from the lungs is of overriding importance for controlling glottic adductor muscle expiratory activity (7, 19).
The aim of the present study was to gain further insight into the
activity of the upper airway muscles, namely the inferior pharyngeal
constrictor, during active expiratory airflow braking in lambs. The
inferior pharyngeal constrictor has not been previously studied in
neonates, and its role in normal and pathological situations, at a
period when upper airway function is so crucial, is unknown. We have
thus recorded inferior pharyngeal constrictor EMG during baseline room
air breathing and during a prolonged period of expiratory airflow
braking triggered by permeability pulmonary edema. The results show
that expiratory airflow braking is accompanied by enhanced expiratory
activity, not only of the thyroarytenoid muscle but also of the
inferior pharyngeal constrictor.
MATERIALS AND METHODS Animals
Surgical Preparation
Surgery was performed under general anesthesia (2% Fluothane and 30% N2O). Under direct vision, we inserted intramuscular bipolar electrodes (enameled chrome wire, 0.7-mm diam; Chromel, Groupe Technique et Scientifique Médicale, Castelnaudary, France) into both the thyroarytenoid and inferior pharyngeal constrictor muscles. Details with regard to electrode insertion into the thyroarytenoid muscle have been described previously (24). For the inferior pharyngeal constrictor, we carefully turned the larynx and inserted the electrode perpendicularly to the muscular fibers attached to the lateral lamina of the thyroid cartilage, near its posterior margin (18). The leads were subcutaneously tunneled to exit on the back of the animals. Electrode placement was confirmed by a systematic autopsy after completion of the experiment.A catheter was inserted in the brachial artery of all lambs for blood gas sampling. Blood gas values were corrected for rectal temperature of each lamb (Mon-a-Therm 6500).
Measurement Apparatus
The measurement apparatus has been described in previous studies (23, 24). Briefly, a face mask, specifically designed for each lamb, was attached to a size 0 pneumotachograph (model 21070B plus model 8815A respiratory integrator, Hewlett-Packard, Waltham, MA). The thyroarytenoid muscle and the inferior pharyngeal constrictor muscle EMG signals were amplified and band-pass filtered at 30-1,000 Hz (model P511 AC preamplifier and model 7DA DC driver amplifier, Grass Quincy, MA) before undergoing a 100-ms moving time averaging (Dept. of Electronics, Faculty of Medicine, University of Sherbrooke, Sherbrooke, PQ, Canada). The integrator used had parallel outputs to a chart recorder and a computer. An eight-channel polygraph (model 7D, Grass) recorded instantaneous airflow, tidal volume (VT), and the raw and integrated EMG signals of both muscles. An IBM-compatible microcomputer (Televideo TeleCAT-286) analyzed the airflow, integrated EMG signals, and inspired O2 fraction at a 40-Hz sampling rate. Collected data were stored on disk for further analysis.Study Design
The design of the study allowed us to infer the role of increased lung water on the expiratory glottic and pharyngeal dynamics in nonsedated lambs.For the study, each unsedated lamb was positioned in a sling. A venous catheter was first inserted under local anesthesia (2% lidocaine) in the superior vena cava through the superficial jugular vein. The face mask was then applied and the head carefully positioned. Each lamb was given at least 10 min to adjust to the mask. After 3 min of room air baseline recording, the lambs were given an intravenous injection of 0.05-0.075 ml/kg halothane over 1-2 min (14). The ambient temperature was kept between 20 and 22°C and the humidity between 50 and 70% throughout the experiments.
Data Analysis
Minute ventilation (
E/kg),
VT
(VT/kg), breathing frequency
(f), and duty cycle
(TI/TT)
were computed for each breath in all lambs. Averages were calculated
over 15 s (i.e., 15-23 breathing cycles) during baseline
recordings and every 30 min postinjection. We looked for expiratory
airflow braking on the flow-volume curves computed breath by breath
during the above-defined 15-s epochs in each lamb. The thyroarytenoid
and the inferior pharyngeal constrictor EMGs were observed throughout
the experimental procedure. The percentage of breaths accompanied by
thyroarytenoid muscle expiratory EMG activity was calculated during the
above-defined 15-s epochs in each lamb. The inferior pharyngeal
constrictor expiratory EMG activity was quantified by averaging the
maximal voltage of the integrated signal over the same 15-s epochs and
expressing the average values as a percentage of the value during
baseline room air breathing (taken as 100%). Finally, average values
for all lambs as a whole were calculated for statistical study.
At the end of the experiment, the lambs were killed, and pulmonary edema was evaluated by macroscopic observation and then by the measurement of lung-to-body weight and wet-to-dry lung weight ratios (33).
Statistical Analysis
Fifteen-second-averaged values for breathing pattern parameters, percentage of cycles with expiratory airflow braking or with thyroarytenoid muscle expiratory EMG activity, and inferior pharyngeal constrictor expiratory EMG activity were compared by analysis of variance for repeated measures, completed by contrast comparison (SuperANOVA 1989, Abacus Concepts, Berkeley, CA).Lung-to-body weight ratio and wet-to-dry lung weight ratio of five of seven lambs with a control group [n = 8; age 15.6 ± 9.5 (SD) days, weight 6.9 ± 2.3 kg] were also compared by a Mann-Whitney test.
RESULTS
The injection of 0.05-0.075 ml/kg halothane induced a response in all lambs but two, which required two and four injections, respectively (total amount 0.125 and 0.2 ml/kg, respectively), before a response was observed. These two lambs behaved like the others thereafter.
Baseline Room Air Breathing
Ventilatory parameters.E,
VT, f, and
TI/TT
during baseline room air breathing are presented in Fig.
1.
E).
Halothane injection (at time 0) was
made at end of baseline period. See text for details.
* P < 0.05.
Thyroarytenoid muscle EMG activity and flow-volume curves. As previously reported in awake nonsedated lambs during baseline room air breathing (22), we observed no expiratory thyroarytenoid muscle EMG activity in the seven lambs studied (Fig. 2). Non-respiratory-related bursts of thyroarytenoid muscle EMG were recorded only during swallowing movements. As in the previous studies by Praud et al. (22-25), no expiratory airflow braking was observed except in one lamb that had 10% of respiratory cycles with expiratory airflow braking in baseline conditions.
TA, moving
time-averaged TA; IPC, raw inferior pharyngeal constrictor muscle EMG
activity; IPC, moving time-averaged inferior
pharyngeal constrictor muscle EMG activity. Inspiration is upward. 
,
Swallowing movement. Note absence of expiratory TA EMG activity and
presence of expiratory IPC EMG activity with a frequent characteristic shape of integrated signal (
).
Inferior pharyngeal constrictor. An expiratory phasic EMG of the inferior pharyngeal constrictor muscle was observed in six of the seven lambs during baseline room air breathing. Its characteristic shape (somewhat variable from 1 breath to another in the same lamb) consisted of an expiratory plateau preceded by an early peak and ending with a second, late expiratory peak (Fig. 2). The seventh lamb had a tonic expiratory EMG of the inferior pharyngeal constrictor muscle. During inspiration, we observed a tonic activity of the inferior pharyngeal constrictor muscle, with an average amplitude of 42 ± 23% of the reference value (baseline expiratory activity) for the seven lambs as a whole.
Response to Halothane Injection
The intravenous injection of halothane induced a permeability pulmonary edema in all lambs, as observed by gross anatomic abnormalities during systematic postmortem examination. Areas of focal hemorrhaging and atelectasis predominant in the dependent portions of the lungs were present with endoluminal foam and bloody pleural liquid. The lung-to-body weight and wet-to-dry lung weight ratios were significantly increased in the halothane group compared with the control group (P < 0.01; Fig. 3). Moreover, a histological analysis performed after hematein, eosin, and safran staining pointed out heterogenous abnormalities, varying from one area to another: vascular congestion and interstitial and/or alveolar edematous hemorrhagic infiltrates. Inflammatory cell accumulation was rarely observed in the pulmonary interstitium.
Early transient response. In six of seven lambs, a prolonged central apnea lasting from 5 to 230 s was observed during the first minutes after injection. Continuous thyroarytenoid and inferior pharyngeal constrictor muscle EMG activity was observed during apneas. Amplitude of both continuous EMGs presented simultaneous variations. Six lambs required rescuing maneuvers, and one lamb died. Prolonged thyroarytenoid and inferior pharyngeal constrictor muscle response. Expiratory airflow braking (usually to zero flow in early expiration) with thyroarytenoid muscle phasic expiratory EMG activity appeared 16 ± 10 min after halothane injection. At the same time, the phasic expiratory EMG of the inferior pharyngeal constrictor muscle significantly increased (P < 0.02; Fig. 4). Thereafter, expiratory flow limitation with both thyroarytenoid and increased inferior pharyngeal constrictor muscle phasic expiratory EMG activities was recorded (for at least 75% of the breaths) throughout the 1.5- to 5-h recording period (Figs. 5 and 6). No increase in inspiratory inferior pharyngeal constrictor EMG activity was observed in any lamb.
, airflow. Inspiration is upward. Note that an active
expiratory glottic and pharyngeal closure (manifested by simultaneous
contraction of thyroarytenoid muscle, inferior pharyngeal constrictor
muscle, and zero airflow during expiration) is present after halothane
injection despite arterial PO2 and pH
near baseline values. Note time correlation between TA EMG activity,
increased IPC EMG activity, and periods of zero airflow during
high-speed recording
(C).
The time course of
E,
VT, f, and
TI/TT
after halothane injection is illustrated in Fig. 1. We observed a
significant and prolonged decrease in
VT
(P < 0.001), f
(P < 0.001), and
TI/TT (P < 0.02), whereas the increase in
E was not
significant (P = 0.15). The time
course of the arterial blood gases and pH
(pHa) recorded in four lambs
(Fig. 7) was variable, with decreased
pHa appearing to be the more
predominant alteration observed.
Effect of blood gas variations on active expiratory airway closure induced by pulmonary edema. Transiently observed hypoxia was corrected spontaneously or with oxygen addition (arterial PO2 >70 Torr or transcutaneous arterial O2 saturation >92%) in all the lambs. Hypoxia correction did not reverse the increased expiratory upper airway muscle EMG activity or expiratory airflow braking in any of the lambs, as illustrated in the example in Fig. 4. Figure 4 also clearly shows that the increased expiratory upper airway muscle EMG activity and airflow braking were observed despite near-baseline values of arterial PCO2 (PaCO2) and pHa.
DISCUSSION
The present study demonstrates that induced permeability pulmonary edema in lambs stimulates the expiratory phasic EMG of both pharyngeal and glottic constrictor muscles with consequent expiratory upper airway closure. The key findings are the following: 1) lambs exhibit a spontaneous and consistent expiratory phasic EMG of the inferior pharyngeal constrictor in baseline conditions, whereas thyroarytenoid muscle expiratory activity is absent; 2) permeability pulmonary edema leads to a significant increase in the expiratory phasic EMG activity of the inferior pharyngeal constrictor, simultaneous to the appearance of active expiratory glottic closure with thyroarytenoid contraction; and 3) hypoxia is not the key factor responsible for the increase in upper airway constrictor muscle expiratory EMG activity during pulmonary edema in lambs.
Inferior Pharyngeal Constrictor Muscle Activity During Baseline Room Air Breathing
The inferior pharyngeal constrictor EMG activity has previously been studied in adult animals of several species and in humans. Most studies have shown a spontaneous expiratory phasic EMG of the inferior pharyngeal constrictor, such as in anesthetized cats (20, 30), rabbits (28), and monkeys (29) and in unanesthetized dogs (15). On the other hand, one study found that unanesthetized rats exhibited an inspiratory EMG of the inferior pharyngeal constrictor (31). In adult humans, a phasic expiratory (and sometimes transitional, from midinspiration to midexpiration) EMG of the inferior pharyngeal constrictor was inconsistently observed during wakefulness (32). The reasons for the discrepancies between these previous results are not known and could be explained by different experimental conditions [use of anesthesia (28), posture (29), presence of tracheostomy (20, 30)] and/or by species differences. Furthermore, the precise studied pharyngeal level was not always well defined, and activity patterns among superior, middle, and inferior pharyngeal constrictor muscles seem to differ from species to species. For example, while the three pharyngeal constrictors are active during expiration in awake humans (32), the expiratory EMG of the inferior pharyngeal constrictor contrasts with the inspiratory firing of the superior and middle pharyngeal constrictors in anesthetized rabbits (28).The present study is the first to describe the inferior pharyngeal constrictor EMG in the neonatal period without anesthetic interference. We observed an expiratory phasic EMG of the inferior pharyngeal constrictor on each respiratory cycle in all but one lamb during baseline conditions. Moreover, we found similar expiratory phasic EMG in 18 other lambs (not involved in the present study) during quiet room air breathing (unpublished observations). Therefore, what would be the purpose of an active expiratory pharyngeal narrowing during quiet breathing in lambs? Contrary to the larynx, the pharynx is a compliant structure submitted to surrounding pressure variations. During expiration, the outflow of expired gas dilates the pharynx and increases physiological dead space. As previously suggested, the inferior pharyngeal constrictor expiratory contraction could stiffen the pharyngeal wall and prevent an increase in dead space (30). The inferior pharyngeal constrictor contraction could also increase expiratory upper airway resistance, either at the pharyngeal level by decreasing the pharyngeal diameter (17) or at the laryngeal level by approximating the hyoid bone and the thyroid cartilage, a mechanism that closes the glottis (5, 16). The increase in expiratory upper airway resistance would consequently induce expiratory airflow retardation and delay lung emptying, helping the neonate to preserve a high end-expiratory lung volume.
Inferior Pharyngeal Constrictor Muscle Activity During Permeability Pulmonary Edema
It has long been observed that human newborns exhibit an expiratory airflow braking during the first minutes after birth (19). This phenomenon is prominent in premature newborns, especially in neonatal respiratory distress syndrome, leading to classic expiratory grunting (8). In a recent study, Hutchison et al. (12) demonstrated that, as in human newborns, nonsedated premature lambs exhibited an expiratory airflow braking with expiratory thryoarytenoid muscle phasic EMG during the first hours of life. Grunting newborns, and especially premature babies, all have in common an excess of lung water (1). In a recent study, we showed that increasing lung water content (by inducing a permeability pulmonary edema) led to an expiratory airflow braking with expiratory thyroarytenoid muscle phasic EMG activity in lambs (24). Both studies suggest that the thyroarytenoid muscle participates to the active expiratory airflow braking in newborn lambs.In a more recent study, Hutchison et al. (13) briefly mentioned that asphyxiated premature lambs exhibited an expiratory phasic EMG of the inferior pharyngeal constrictor muscle simultaneous to the expiratory thyroarytenoid muscle EMG and airflow braking in the first minutes after birth. In keeping with this observation, the present study shows that pharyngeal and laryngeal constrictor muscles can be stimulated simultaneously in experimental conditions mimicking neonatal respiratory problems. While increased inferior pharyngeal constrictor muscle EMG activity could serve to stiffen the pharyngeal wall during increasing airflow, the accompanying upper airway closure with zero flow during expiration recorded in all our lambs is likely related to the enhanced activity of both pharyngeal and laryngeal constrictor muscles. Indeed, it has been previously shown that active laryngeal closure involves intrinsic and extrinsic laryngeal muscles (16) and that the inferior pharyngeal constrictor muscle is considered to be an extrinsic laryngeal muscle: by pulling the thyroid cartilage toward the hyoid bone, it contributes to laryngeal closure (5, 16). Thus we speculate that the increase in expiratory phasic EMG of the inferior pharyngeal constrictor acts together with expiratory thyroarytenoid muscle contraction to produce an expiratory glottic closure with zero flow during high-permeability pulmonary edema in lambs. Furthermore, we speculate that a similar mechanism involving both thyroarytenoid and inferior pharyngeal constrictor muscle operates in premature babies with expiratory grunting.
Origin of the Increase in Pharyngeal Constrictor Muscle Activity
The mechanism(s) linking permeability pulmonary edema to increased pharyngeal constrictor muscle expiratory activity in lambs is unknown. Several possible factors may involve chemo- or mechanoreceptors.As previously shown for glottic constrictor muscle (12, 22-25), hypoxia in the present study does not appear to be a key factor. Indeed, correction of hypoxia (either spontaneously or with O2 administration) during pulmonary edema did not decrease the expiratory EMG activity of the inferior pharyngeal constrictor. Likewise, while acidosis and slight hypercapnia were observed in the four studied lambs as a whole, increased inferior pharyngeal constrictor muscle EMG activity was also recorded in the presence of normal arterial pH and PaCO2 (see Fig. 4), similar to previous findings in preterm lambs for thyroarytenoid muscle EMG (12). Thus, although we cannot rule out that increased PaCO2 could have participated in the enhancement of expiratory inferior pharyngeal constrictor EMG (30, 32), this does not seem to be a prerequisite in lambs with pulmonary edema.
Reflex mechanisms originating from mechanoreceptors in the lower respiratory apparatus could enhance inferior pharyngeal constrictor muscle activity during pulmonary edema, as for the glottic constrictor muscles. Indeed, previous data have shown that glottic constrictor muscle expiratory activity depends on lung receptive feedback and is important in maintaining end-expiratory lung volume (7, 19). Pulmonary edema decreases lung compliance and hence lung volume. Consequent decrease in afferent messages from slowly adapting receptors could thus enhance both glottic and inferior pharyngeal constrictor muscle expiratory contraction. On the other hand, stimulation of C-fiber endings and rapidly adapting receptors have been shown during pulmonary edema (21, 26, 27), and C-fiber ending stimulation by capsaicin increases glottic constrictor activity (9, 11). Finally, stimulation of pulmonary arterial baroreceptors (by increased pulmonary arterial pressure) may also be involved (3). Thus vagally mediated afferent activity originating from mechanoreceptors in the respiratory apparatus is likely important in enhancing upper airway constrictor muscle activity during pulmonary edema. However, previous data on the effect of vagotomy upon pharyngeal constrictor muscle activity are scarce and contradictory (30) and preclude any firm conclusions.
In summary, the results of the present study, along with previous data from our laboratory, show that the electrical activity of both thyroarytenoid and inferior pharyngeal constrictor muscle in lambs is enhanced in a situation with permanent expiratory airflow braking. We hypothesize that this essential defense strategy in newborn infants involves similar upper airway muscle activity, mainly triggered by the excess of lung water present at birth.
ACKNOWLEDGEMENTS
The authors acknowledge the expert secretarial assistance of Carole Jacques in the preparation of the manuscript.
FOOTNOTES
Address for reprint requests: J.-P. Praud, Dept. of Pediatrics and Pulmonary Research Unit, Faculty of Medicine, Univ. of Sherbrooke, Sherbrooke, Quebec J1H 5N4, Canada.
Received 13 October 1995; accepted in final form 23 May 1996.
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I-J. Lu, K.-Z. Lee, and J.-C. Hwang Capsaicin-induced activation of pulmonary vagal C fibers produces reflex laryngeal closure in the rat J Appl Physiol, October 1, 2006; 101(4): 1104 - 1112. [Abstract] [Full Text] [PDF]
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I-J. Lu, K.-Z. Lee, J.-T. Lin, and J.-C. Hwang Capsaicin administration inhibits the abducent branch but excites the thyroarytenoid branch of the recurrent laryngeal nerves in the rat J Appl Physiol, May 1, 2005; 98(5): 1646 - 1652. [Abstract] [Full Text] [PDF]
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V. Diaz, D. Dorion, I. Kianicka, P. Letourneau, and J.-P. Praud Vagal afferents and active upper airway closure during pulmonary edema in lambs J Appl Physiol, May 1, 1999; 86(5): 1561 - 1569. [Abstract] [Full Text] [PDF]
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V. Diaz, D. Dorion, S. Renolleau, P. Letourneau, I. Kianicka, and J.-P. Praud Effects of capsaicin pretreatment on expiratory laryngeal closure during pulmonary edema in lambs J Appl Physiol, May 1, 1999; 86(5): 1570 - 1577. [Abstract] [Full Text] [PDF]
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 S. RENOLLEAU, P. LETOURNEAU, T. NIYONSENGA, J.-P. PRAUD, and B. Gagne Thyroarytenoid Muscle Electrical Activity During Spontaneous Apneas in Preterm Lambs Am. J. Respir. Crit. Care Med., May 1, 1999; 159(5): 1396 - 1404. [Abstract] [Full Text] [PDF]
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