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Department of Biomedical Sciences, Creighton University School of Medicine, Omaha, Nebraska 68178; and Laboratory for Exercise and Environmental Medicine, Health, Leisure, and Human Performance Research Institute, University of Manitoba, Winnipeg, Manitoba, Canada R3T 2N2
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Pisarri, Thomas E., and Gordon G. Giesbrecht. Reflex
tracheal smooth muscle contraction and bronchial vasodilation evoked by
airway cooling in dogs. J. Appl.
Physiol. 82(5): 1566-1572, 1997.
Cooling
intrathoracic airways by filling the pulmonary circulation with cold
blood alters pulmonary mechanoreceptor discharge. To determine whether
this initiates reflex changes that could contribute to airway
obstruction, we measured changes in tracheal smooth muscle tension and
bronchial arterial flow evoked by cooling. In nine
chloralose-anesthetized open-chest dogs, the right pulmonary artery was
cannulated and perfused; the left lung, ventilated separately, provided
gas exchange. With the right lung phasically ventilated, filling the
right pulmonary circulation with 5°C blood increased smooth muscle
tension in an innervated upper tracheal segment by 23 ± 6 (SE) g
from a baseline of 75 g. Contraction began within 10 s of injection and
was maximal at ~30s. The response was abolished by cervical vagotomy.
Bronchial arterial flow increased from 8 ± 1 to 13 ± 2 ml/min, with
little effect on arterial blood pressure. The time course was
similar to that of the tracheal response. This response was greatly
attenuated after cervical vagotomy. Blood at 20°C also increased
tracheal smooth muscle tension and bronchial flow, whereas 37°C
blood had little effect. The results suggest that alteration of
airway mechanoreceptor discharge by cooling can initiate reflexes that
contribute to airway obstruction.
cold air; exercise-induced asthma; bronchial artery; pulmonary
mechanoreceptors; bronchoconstriction; lung innervation; vagus nerve; airway resistance
INTRODUCTION IN ASTHMATIC INDIVIDUALS, hyperventilation,
particularly with cold dry air, can result in airway obstruction
(10). However, despite many human and animal studies,
neither the transduction mechanism of the cold, dry stimulus nor the
effector mechanism that produces the obstruction has been clearly
identified. Most explanations of the initiating stimulus focus on
either the direct cooling effect of the inspired air or on the
increased osmolarity of the airway surface liquid that accompanies
humidification of the inspired air (12). The relative importance of
these two components of the stimulus has been difficult to separate
because, on the one hand, cold air necessarily is dry and, on the other hand, the evaporation that occurs during ventilation with even warm dry
air inevitably cools the airway.
The pathways by which either drying or cooling causes obstruction
remain uncertain. Increasing osmolarity of the airway lining has been
hypothesized to act through stimulation of afferent nerves (23, 27) or
through release of mediators from airway mast cells (3), both of which
can induce bronchoconstriction, bronchial vasodilation, plasma
extravasation, and mucus secretion. Airway cooling has been
hypothesized to act locally on the airway vasculature to cause
vasoconstriction followed by reactive hyperemia that narrows the lumen
(20). However, this may not be the sole mechanism by which cooling
produces obstruction. Localized tracheal cooling, without drying,
reduces external tracheal diameter, implying tracheal smooth muscle
contraction rather than submucosal engorgement (11). Moreover, airway
cooling, even in the absence of drying, alters the discharge of lower
airway mechanoreceptors (16), an effect potent enough to alter
the pattern of breathing (17). Because these same airway
mechanoreceptors influence airway smooth muscle tone, cooling
could produce obstruction through neural mechanisms (25).
Therefore, in the present study, we measured the effect of cooling the
intrapulmonary airways on tracheal smooth muscle tension and bronchial
arterial flow before and after eliminating neural pathways by cutting
the vagus nerves. To avoid concomitant drying of the airway, we cooled
the airways of the right lung by filling the right pulmonary vessels
with cold blood. Because the effect of cold on afferent discharge
depends on lung volume (16), we examined the responses to cooling both
during phasic ventilation and with the right lung held at both low and
high constant volumes.
METHODS
-chloralose (80 mg/kg iv). Supplementary doses of -chloralose (10 mg/kg iv) were given hourly to maintain surgical anesthesia.
br) evoked by filling right pulmonary circulation with blood at indicated temperatures. Phasic ventilation of right lung is indicated by right bronchial pressure (Prbr) excursions. Point at which right pulmonary arterial flow was stopped is indicated by drop in right pulmonary arterial pressure (Prpa; first arrow on trace). One minute later, blood was
injected, indicated by event marks (bars) on time traces and by
transient elevation of Prpa. Pulmonary arterial flow was resumed 1 min
later (second arrow on Prpa trace). Order of injection of boluses of
the 3 temperatures was randomized.
To examine the effect of lung volume on the response to cooling, we injected blood at 5, 20, and 37°C while the static inflation pressure of the right lung was set, in random order, at 5 and 15 cmH2O. In these experiments, pulmonary arterial perfusion was stopped only after tension and flow had stabilized after the step change in airway pressure. Finally, in seven of the dogs, injection of 5°C blood was repeated after the cervical vagus nerves were cut bilaterally. The effect of vagotomy on the bronchial arterial response was measured in each of these dogs. The effect on the tracheal smooth muscle response was examined only in the six dogs in which a response to cold blood remained after we cut the recurrent and pararecurrent laryngeal nerves, which supply some of the motor innervation of tracheal smooth muscle but are interrupted by cervical vagotomy. After the recurrent nerves were cut, the motor innervation of the trachea (from the superior laryngeal nerves) is not further reduced by subsequent cervical vagotomy; therefore, elimination of the response could be attributed solely to interruption of vagal afferents. Analysis of results. Control tension and flow were measured with the right pulmonary arterial perfusion stopped over the 30 s preceding each injection. The response to injection was measured as the maximal change in the period between injection and the restoration of vascular perfusion. Results are expressed as means ± SE. Statistical significance of the responses, comparisons of the response to blood at different temperatures, and comparisons to injection of cold (5°C) blood at different airway pressures were made by using analysis of variance (ANOVA) for repeated measures. If a significant effect was detected, individual means were compared by constructing contrasts by using SuperANOVA statistical software. If the data were not normally distributed, a nonparametric test (Wilcoxon signed-rank test) was used. Statistical significance was accepted if P < 0.05.
RESULTS
Ttr) from baseline caused by
filling right pulmonary circulation with blood at indicated temperatures in 9 dogs during phasic ventilation of right lung. 
,
Control averaged over 60 s before injection; 
, peak response. Response significantly different from response to 37°C blood: * P < 0.05;
** P< 0.01.
Bronchial arterial flow increased in response to injection of 5 and 20°C blood, by 76 ± 16% after injection of blood at 5°C, whereas 37°C blood had no effect (Figs. 1 and 3). Injection of cold blood had negligible effects on arterial pressure (which increased by 0.5 ± 2.7, 3.2 ± 2.5, and 2.6 ± 1.9 mmHg with injection of 5, 20, and 37°C blood, respectively). Thus the increases in bronchial arterial flow reflect increases in bronchial vascular conductance.
br before () and at peak
response to () filling right pulmonary circulation with blood at
indicated temperatures in 8 dogs during phasic ventilation of right
lung. Control was averaged over 60 s before injection. Response
significantly different from response to 37°C blood:
** P < 0.01;
*** P < 0.001.
Lung inflated at constant pressure. In eight of these dogs we repeated the cold-blood injections with the right lung held constant at 5 and 15 cmH2O transpulmonary pressure to determine the effect of lung volume on the response. Increasing the transpulmonary pressure from 5 to 15 cmH2O slightly reduced the baseline tracheal smooth muscle tension; baseline tension was readjusted to 75 g before each injection of blood. Injection of 5°C blood significantly increased tracheal tension at both high and low lung volumes, but the effect of 20°C blood was significant only at the higher lung volume (Figs. 4 and 5). At 15 cmH2O, the tracheal contraction evoked by filling the right pulmonary circulation with 5 and 20° blood was enhanced by >25% in six of the eight animals compared with the same stimulus at 5 cmH2O.
br evoked by filling right pulmonary circulation with 20°C blood. Note that at higher airway pressure, Ttr response is enhanced while br response is slightly reduced.
Ttr from baseline caused by filling right
pulmonary circulation with blood at indicated temperatures in 8 dogs
with inflation pressure of right lung held constant at 5 or 15 cmH2O. , Control averaged over
60 s before injection; , peak response. Peak significantly greater
than control: *P < 0.05;
** P < 0.01.
The increase in static lung volume often caused a transient decline in bronchial blood flow that recovered within 1 or 2 min. Injection of either 5 or 20°C blood significantly increased bronchial blood flow at both high and low lung volumes (Figs. 4 and 6). At the higher lung volume, the vasodilation evoked by injection of 5°C blood was slightly smaller than at the lower volume (P < 0.02; Fig. 6).
br before () and at peak
response to () filling right pulmonary circulation with blood at
indicated temperatures in 7 dogs with inflation pressure of right lung
held constant at 5 or 15 cmH2O.
Control was averaged over 60 s before injection. ** Peak
significantly greater than control, P < 0.01. 
Response at 15 cmH2O significantly different from
response at 5 cmH2O,
P < 0.05.
Injection of 37°C blood had no effect on either tension or flow at either lung volume. Effect of vagotomy. Bilateral cervical vagotomy abolished the tracheal smooth muscle contraction and greatly reduced the bronchial vasodilation (Figs. 7 and 8). Cutting the cervical vagus nerves to interrupt afferent conduction from the lungs abolished the bronchoconstriction in each of six dogs in which a tracheal smooth muscle response remained after the recurrent laryngeal nerves were cut. The effect of vagotomy on the reflex vasodilation was more variable. In two dogs, vagotomy abolished the bronchial vasodilation; in the five others, it was greatly attenuated (to 38 ± 5% of the prevagotomy response).
br is greatly attenuated but not
abolished.
Ttr (A) from
baseline and br
(B) before (open symbols) and at
peak response to (filled symbols) filling right pulmonary circulation
with 5°C blood before (circles) and after (squares) cutting
cervical vagus nerves. Control was averaged over 60 s before injection.
Prevagotomy response was measured with recurrent laryngeal nerves cut.
Peak significantly greater than control:
* P < 0.05;
*** P < 0.001.
DISCUSSION
Cooling the lower airways by decreasing the temperature of pulmonary arterial blood, thereby avoiding changes in the osmolarity of the airway surface liquid, increased both airway smooth muscle tension and bronchial blood flow. The intensity of the effect was proportional to the degree of cooling; injection of blood at 5°C caused the greatest changes, blood at 20°C caused smaller changes, and blood at body temperature had no effect. The evidence suggests that the tracheal smooth muscle contraction and most of the bronchial vasodilation were due to a reflex having an afferent limb that traveled in the vagus nerve.
Tracheal contraction. In the case of the tracheal smooth muscle, only a reflex effect is possible. The isolated tracheal segment itself was not cooled by the cold blood, which remained in the right pulmonary circuit throughout the response. Communication between the cooled lower airway and the tracheal smooth muscle could occur only through neural pathways passing through the central nervous system to the parasympathetic efferents to the trachea. The afferent pathway is in the vagus nerve, because bilateral cervical vagotomy abolished the response; the efferent parasympathetic pathway through the superior laryngeal nerve remains intact after cervical vagotomy. Reflex smooth muscle contraction could be initiated by stimulation of rapidly adapting pulmonary stretch receptors, by reduced discharge of slowly adapting pulmonary stretch receptors, or by both. Although stimulation of the afferent endings of vagal sensory C fibers in the lung and airways evokes tracheal smooth muscle contraction (9), these afferents are not significantly affected by injection of cold blood (16) and hence are unlikely to contribute to the cold-evoked response. Rapidly adapting receptors are stimulated by injection of cold but not of warm blood, and the stimulation is enhanced at higher lung volume (16). These receptors are widely believed to initiate reflex airway contraction (8, 24, 28), although the interpretation of the evidence is controversial (7, 8). Thus cold-induced tracheal smooth muscle contraction could be initiated by rapidly adapting receptor stimulation. Cold-blood injection might also cause tracheal smooth muscle contraction by reducing the afferent activity of slowly adapting receptors, which inhibit the vagal bronchomotor neurons responsible for resting airway smooth muscle tone (8, 28). During phasic ventilation, the injection of cold blood reduces transmission of slowly adapting receptor input to the central nervous system (16). The net effect of cold on slowly adapting receptors results from the interaction of two opposing influences: cold reduces the maximal frequency of axon discharge but also directly stimulates the receptors. At high lung volumes, when the discharge frequency of most slowly adapting receptors is high, the axonal effect predominates and reduces input from these receptors. At low lung volumes, the opposing effects may cancel out, producing no net change in slowly adapting stretch receptor input (16). In the present experiments, holding the right lung at high volume enhanced the airway smooth muscle response to cold in most animals compared with holding the lung at low volume, a result consistent with mediation by inhibition of slowly adapting receptor activity. However, because baseline smooth muscle tone is reduced by the increased inhibition of vagal bronchoconstrictor efferents at the higher lung volume, the enhanced response may be influenced by changes in the resting muscle length and, therefore, may not exclusively reflect increased inhibition of the slowly adapting receptor input. Moreover, because the stimulation of rapidly adapting receptors by cold is also enhanced at high lung volumes (16), we cannot estimate the relative contribution of the two receptors to the tracheal smooth muscle response. Although cooling confined to the central airways can evoke airway smooth muscle contraction (11, 29), contraction elicited by cooling the intrathoracic airways has not previously been demonstrated. Indeed, perfusion of the left lower lobe with 30°C blood for 2 min had little direct effect on peripheral airway resistance (14) and actually attenuated the increase in peripheral airway resistance evoked by cold airflow or hypertonic saline aerosol but not the direct effect of histamine aerosol (13, 15). The design of the above-mentioned studies by Freed and colleagues (13-15) makes them more likely to detect local effects of cold, whereas the present study was optimized to detect reflex effects. In the studies of Freed and colleagues, cooling was confined to a single lung lobe maintained at low distending pressure. Both the limited area of cooling and the low baseline mechanoreceptor discharge (at the low lung volume) would limit the effect of cooling on mechanoreceptor afferent input. In contrast, our study directly cooled an entire lung at normal volume. Second, Freed et al. measured resistance in airways that were directly cooled, whereas we measured the contraction of tracheal smooth muscle that was not cooled (because it was perfused by the body temperature blood of the systemic circulation). Because cooling reduces the contractile response of tracheal (4) and bronchial (19) smooth muscle to cholinergic agonists or electrical field stimulation in vitro, reflex contraction in the lower airway could be opposed by direct cooling. Nonetheless, the small but consistent increase in peak right airway pressure we observed suggests that contraction of the airway smooth muscle did occur in the cooled lobe. Finally, because Freed et al. continuously pumped cold blood through the open pulmonary circuit, some systemic cooling may have occurred. In the present study, cold blood injected into the pulmonary circuit did not enter the systemic circuit until perfusion was reestablished after the period of measurement. Taken together, the results suggest that cold acts through neural pathways to cause bronchoconstriction that may be opposed by local effects of cooling, particularly in the lower airways. Bronchial vasodilation. The genesis of the bronchial vasodilation evoked by cooling is more obscure. Because the vasodilation was greatly attenuated by cervical vagotomy, much of the response can be attributed to a reflex. Cervical vagotomy eliminates both the lung and airway afferents and the efferent vagal parasympathetic vasodilator fibers, which mediate most of the reflex bronchial vasodilation in anesthetized dogs (6). Therefore, the attenuation indicates that the afferent or efferent reflex pathways, or both, travel in the vagus nerve. The identity of the vagal afferents that might mediate the reflex vasodilation is uncertain. As discussed earlier (see Tracheal contraction), the discharge of both slowly and rapidly adapting pulmonary stretch receptors, but not pulmonary C fibers, is altered by cooling (16); however, there is little evidence for a reflex effect of either type of mechanoreceptor on bronchial vascular resistance. A bronchial vasodilator effect of rapidly adapting receptor stimulation is suggested by the observation that injection of water in the airway, a strong stimulus to rapidly adapting receptors (23), evokes reflex bronchial vasodilation (22). However, the role of rapidly adapting receptors in the water-evoked vasodilation cannot be confirmed because water also stimulates lung and airway C fibers (23). If rapidly adapting receptor stimulation alone were responsible for the cold-evoked vasodilation, we would have expected enhanced vasodilation at high static airway pressure, which increases the stimulation of rapidly adapting receptors by cold blood (16). This did not occur; indeed, the vasodilation was somewhat reduced at higher pressures. However, increasing airway pressure exerts physical effects on the bronchial vessels that may oppose any reflex vasodilation (1). An additional possibility is that metabolic vasodilation, secondary to bronchial airway smooth muscle contraction, contributes to the vagally dependent vasodilation. Thus the exact vagal pathways that mediate the vasodilation remain uncertain. The mechanism by which hyperventilation of dogs with cold or dry air increases tracheal and bronchial blood flow (5) has never been satisfactorily resolved (26). Airway drying was felt to be more important than airway cooling in the hyperventilation-evoked vasodilation (5), and previous experiments have provided little evidence of cold-evoked reflex airway vasodilation in dogs in the absence of drying. Instillation of cold isotonic saline into the trachea of dogs increased tracheal vascular conductance by only 6% (11), in contrast to the 75% increase in bronchial vascular conductance in the present study. We do not know whether the difference resulted from the different means of delivering the cold stimulus or from a difference between tracheal and bronchial circulation. In a study of the lower airway vasculature, perfusion of the isolated pulmonary circulation to a single lung lobe with cold blood decreased systemic (i.e., bronchial) flow to the lobe (2). Because the cold stimulus and the flow measurement were confined to the same lobe, reflex effects would be less prominent than in our experiments, in which the stimulus was delivered to only one lung while we measured the entire bronchial arterial flow. However, a difference between local and reflex effects cannot fully account for the differences between the studies. After vagotomy, which removed the reflex component of the vasodilation, we did not observe an unmasked local vasoconstriction. The difference may be in part due to the higher sensitivity of our protocol to acute, rapid effects. Whereas we measured flow continuously in response to 1-min decreases in temperature, the earlier study (2) averaged flow in 5-min intervals over 30 min of cooling. Relevance to the airway defense response and hyperpnea-induced airway obstruction. The neural reflexes we have described are undoubtedly important in protecting the lower airways. Physiologically, airway cooling signals the presence of air that has not been completely conditioned. Bronchoconstriction and bronchial vasodilation, by simultaneously reducing ventilation and increasing mucosal blood flow, restore the balance between inspiratory airflow and availability of heat and moisture to condition it. Cooling might also signal the presence in the airway of an exogenous, potentially noxious, substance, because an inhaled liquid or solid would not be warmed as rapidly as air. Bronchoconstriction would limit the entry of the potential irritant while increased bronchial flow would be the first step in an inflammatory process to neutralize the irritant and repair any damage it produced. In hypersensitive individuals, these same reflex pathways could contribute to hyperpnea- or cold-induced airway obstruction. Filling the right pulmonary circulation with 5 and 20°C blood lowers the right lung temperature to ~30 and 33°C respectively (16, 17), temperatures that have been reported in the walls of subsegmental bronchi during hyperventilation with cold air (18). Thus, even in the absence of drying, temperatures that provoke airway obstruction in asthmatic individuals can evoke reflex bronchoconstriction and vasodilation, both of which contribute to airway obstruction. Pisarri et al. (21-23) have previously shown that changes in airway osmolarity, in the absence of temperature change, evoke similar reflex responses mediated by stimulation of airway and pulmonary C fibers and rapidly adapting receptors. Together, these studies suggest that regardless of whether airway cooling or airway drying initiates the airway obstruction, reflexes elicited by airway afferents may contribute. Clearly, these mechanisms by themselves do not explain hyperpnea- or cold-induced airway obstruction. Because both the cold-sensitive and osmolarity-sensitive reflex pathways were demonstrated in mixed-breed "nonasthmatic" dogs, the mere presence of the reflex pathways is not sufficient to cause obstruction. The observation that exercise-induced airway obstruction in susceptible individuals occurs only after the end of exercise suggests that the abnormality involves an imbalance between obstructive pathways, such as those we have demonstrated, and protective mechanisms, such as the bronchodilating effects of circulating catecholamines. While obstructive and protective mechanisms have a similar time course in normal individuals, asthma may result from prolongation of the obstructive influences beyond the termination of the protective influences.ACKNOWLEDGEMENTS
We thank Albert Dangel and Ronald Brown for technical assistance.
FOOTNOTES
Address for reprint requests: T. E. Pisarri, Dept. of Biomedical Sciences, Creighton Univ. School of Medicine, Omaha, NE 68178 (E-mail: tpisarri{at}creighton.edu).
Received 8 October 1996; accepted in final form 17 December 1996.
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