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Published ahead of print on July 8, 2004, doi:10.1164/rccm.200312-1691OC
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American Journal of Respiratory and Critical Care Medicine Vol 170. pp. 780-785, (2004)
© 2004 American Thoracic Society
doi: 10.1164/rccm.200312-1691OC

Original Article

Quantitative Assessment of Tracheal Collapsibility in Infants with Tracheomalacia

Junko Okazaki, Shiroh Isono, Hisaya Hasegawa, Miho Sakai, Yuzo Nagase and Takashi Nishino

Department of Anesthesiology (B1), Graduate School of Medicine, Chiba University, Chiba; Department of Neonatology; and Department of Cardiovascular Surgery, Matsudo City Hospital, Matsudo, Japan

Correspondence and requests for reprints should be addressed to Shiroh Isono, M.D., Department of Anesthesiology (B1), Graduate School of Medicine, Chiba University, 1-8-1 Inohana-cho, Chuo-ku, Chiba, 260–8670, Japan. E-mail: isonos{at}ho.chiba-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Infantile tracheomalacia is a potentially life-threatening disease requiring prolonged artificial respiratory support. Diagnosis and management of this disease may be further improved by establishing a suitable objective and quantitative assessment protocol for tracheal collapsibility. It is our hypothesis that tracheal collapsibility can be represented by the relationship between intraluminal pressure and the cross-sectional area of the trachea. To test this hypothesis, static pressure/area relationships of the trachea were obtained from anesthetized and paralyzed infants, who were diagnosed as having tracheomalacia by endoscopic observation. These relationships were fitted on a linear regression model, followed by calculation of the estimated closing pressure. The tracheal closing pressure ranged from –8 to –27 cm H2O, suggesting easy collapsibility of the trachea during crying or coughing and noncollapsibility during the spontaneous respiratory cycle, which coincided with the infants' symptoms. It is our conclusion that tracheal collapsibility of infants with tracheomalacia can be quantitatively assessed by the static pressure/area relationship of the trachea obtained under general anesthesia and paralysis.

Key Words: anesthesia • closing pressure • endoscopy • paralysis • tube law

Infantile tracheomalacia is a potentially life-threatening disease. Increased positive intrathoracic pressure produced during crying or coughing in infants with tracheomalacia occasionally develops obstruction of the collapsible trachea (1), inducing a sudden onset of obstructive apnea or distressed breathing, which often requires resuscitation when it prolongs and leads to severe cyanosis (dying spell). Prolonged artificial respiratory support with high positive end-expiratory pressure is necessary until the tracheal collapsibility improves with maturation or is surgically corrected.

Recent technical advancement of the ultrathin endoscope has significantly improved diagnosis of infantile tracheomalacia. Diagnosis is usually based on the observation of dynamic tracheal narrowing during increased expiratory efforts. However, because the magnitude of increased intrathoracic pressure during the evaluation is apt to vary not only between individuals but even within one individual, the current endoscopic assessment of tracheal collapsibility is highly subjective and it is still sometimes difficult to differentiate tracheomalacia from tracheal stenosis. The development of a suitable objective and quantitative assessment protocol for tracheal collapsibility may aid in improving the diagnosis and management of the disease.

We hypothesized that the trachea collapses when transmural pressure of the trachea changes, which may be represented by the relationship between intraluminal pressure and cross-sectional area of the trachea. In this study, static pressure/area relationships of the trachea in anesthetized and paralyzed infants with tracheomalacia were obtained, and we tested whether the relationship quantitatively describes collapsibility of the trachea in these infants.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
The study consisted of eight infants with tracheomalacia (Tables 1 and 2) and four infants without tracheomalacia (Table 3). All infants with tracheomalacia demonstrated a cyanotic spell associated with crying. The diagnosis was made by endoscopic observation of apparent tracheal narrowing or obstruction during crying. Three were diagnosed as having bronchomalacia in addition to tracheomalacia. An airway was intubated, and mechanical ventilation with high positive end-expiratory pressure or continuous positive airway pressure was necessary to prevent life-threatening respiratory events in six infants (Table 2).


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  		TABLE 1. Anthropometric characteristics and coexisting diseases for each infant with tracheomalacia

 

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  		TABLE 2. Clinical symptoms and treatments of the tracheomalacia for each infant with tracheomalacia

 

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  		TABLE 3. Anthropometric characteristics and coexisting diseases for each infant without tracheomalacia

 
To test further the validity of the static pressure/area measurements of the trachea in infants without tracheomalacia, we invited to participate in this study four infants who were intubated but had no symptom suggesting tracheomalacia (Table 3). Three infants had respiratory disorders immediately after delivery but recovered from them (n = 3), and one was scheduled to have a minor surgery under general anesthesia (n = 1). Our institutional ethics committee approved the study. The aim and potential risks of this study were fully explained to the parent(s), and informed consents were obtained.

Experimental Setting
Each infant was anesthetized and paralyzed by intravenous injection of midazolam (0.3–0.5 mg/kg) and pancuronium (0.1–0.2 mg/kg) or vecuronium (0.1–0.2 mg/kg) (Figure 1). One infant without tracheomalacia (N4) was anesthetized with sevoflurane and nitrous oxide in oxygen and paralyzed by vecuronium for the surgery. Atropine sulfate (0.01 mg/kg) was administered intravenously to reduce airway secretion. Two infants not requiring mechanical ventilation before this study (T7 and T8) were anesthetized and intubated for this study. Appropriate endotracheal tube size not eliciting air leak at an increased airway pressure of 15 cm H2O was selected, and the tip of the tube was adjusted to place just below the larynx for the tracheal evaluation, minimizing influences of the endotracheal tube on the collapsibility of the trachea.



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  		Figure 1. Experimental setting for measurements of static pressure/area relationship of the trachea in anesthetized and paralyzed infant with an endotracheal tube. ET = endotracheal tube; Paw = airway pressure, VCR = video cassette recorder.

 
All infants were mechanically ventilated with the appropriate inspired oxygen fraction to avoid hypoxemia and hyperoxemia. An electrocardiogram was monitored, and SaO2 was measured by pulse oximeter throughout the experiment.

A thin fiberoptic bronchoscope (1.8 mm outer diameter, MS551; d-Base, Tokyo, Japan) connected to a video recording system was inserted through a diaphragm of an elbow connector at the junction of the endotracheal tube without air leak. The endotracheal tube was connected to a pressure controller, capable of producing a constant, preselected airway pressure (Paw) ranging from +10 to –10 cm H2O in steps of 1 cm H2O. Reading of Paw, measured by a water manometer, was simultaneously recorded on the videotape.

Experimental Procedure
Cessation of mechanical ventilation resulted in apnea caused by muscle paralysis. Paw was immediately increased and maintained at 10 cm H2O. Although the infant remained apneic for 30–40 seconds, Paw was slowly reduced from +10 to –10 cm H2O in a stepwise fashion (1 cm H2O for each step). Maintenance of each test pressure for approximately 1 second during the apnea made the pressure along the airway equal, and therefore, the Paw is considered to be equal to the pressure at the tracheal segment where we measured the cross-sectional area. This allowed measurements of static pressure–area relationship of the trachea (apneic test). The Paw was always changed in the same direction during the apneic test. We dilated the airway first and observed a reduction of the cross-sectional area to avoid the hysteresis possibly caused by surface tension (2). Pressure/area relationships of the main bronchus were obtained in bronchomalacia cases. Measurement was suspended at onset of SaO2 decrease to 90%, followed by mechanical ventilation of the patient to full pre-evaluation SaO2 value. The recorded images were digitized and stored in a computer for later analysis of tracheal cross-sectional area using computer software.

Data Analyses
To measure the tracheal cross-sectional area, digitized tracheal images were traced by a computer software (SigmaScan version 2.0; Jandel Scientific Software, San Rafael, CA). Fraction to cross-sectional area at Paw of +10 cm H2O (FAtr) was calculated for each Paw. The FAtr was plotted as a function of Paw (Paw/FAtr relationship). The Paw/FAtr relationship was fitted on a linear regression model, FAtr = A · Paw + B, where A and B are constants. The quality of the fitting was provided by coefficient R2 (SigmaPlot 2000 for Windows, version 6.00). An intercept of the Paw axis that was extrapolated by the linear model was defined as the estimated closing pressure of the trachea (P'close = –B/A). The percentage of reduction of tracheal cross-sectional area from Paw of 10 to –10 cm H2O was also calculated (100 · [1 – {FAtr at Paw of –10 cm H2O}]). Complete closure of the trachea during testing was denoted as a 100% reduction. The correlation between the variables was assessed by a Spearman correlation analysis, where p < 0.05 was considered to be significant.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Static pressure/area relationships of the trachea were successfully obtained in all infants. During testing, mild hypoxemia and SaO2 decrease to nearly 80% developed in two infants, whereas the other infants maintained an SaO2 of greater than 90%. Bradycardia was not observed, and desaturation was reversed after resumption of mechanical ventilation.

An Example of Static Pressure/Area Relationship of the Trachea
Figure 2 presents an example of endoscopic tracheal images and static pressure/area relationship in an infant with tracheomalacia. As Paw decreased from 10 to –10 cm H2O, the tracheal posterior membrane approached anterior cartilaginous ring, resulting in a prominent decrease of the cross-sectional area of the trachea. The cross-sectional area of the trachea was reduced by 78% when intratracheal pressure decreased from 10 to –10 cm H2O. Static pressure/area data were fitted on a linear regression model with a high R2 value (R2 = 0.970). P'close was calculated as –15 cm H2O.



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  		Figure 2. An example of intratracheal images and static pressure/area relationship of the trachea in an infant with tracheomalacia. The tracheal posterior membrane approached the anterior cartilaginous ring, resulting in a prominent decrease of the cross-sectional area of the trachea at lower airway pressures. Static pressure/area data were fitted on a liner regression model with a high R2 value (R2 = 0.970). P'close was calculated as –15 cm H2O.

 
Results of Static Pressure/Area Assessment in Infants with Tracheomalacia
Results of the fitting analyses of pressure/area relationships of the trachea for all the infants with tracheomalacia are presented in Table 4. P'close ranged from –8 to –27 cm H2O. High R2 values indicate validity of the linear regression model for the Paw range of 10 to –10 cm H2O. The cross-sectional area of the trachea was reduced by more than 50% in all infants.


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  		TABLE 4. Results of fitting analysis for each infant with tracheomalacia on a linear regression model and percentage reduction of the cross-sectional area of the trachea

 
A significant dependency of P'close on body weight (R = –0.762, p = 0.02) was found, whereas no correlation was evident between P'close and postconceptional age, age, and birth body weight (Figure 3).



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  		Figure 3. Relationship between body weight and tracheal P'close. A significant dependency of P'close on body weight (R = –0.762, p = 0.02) was found.

 
Bronchial Pressure/Area Relationships and P'close
Bronchial pressure/area relationships of three infants presenting apparent bronchial narrowing during diagnostic endoscopic evaluation (left main bronchus in cases 4 and 7, right main bronchus in case 8) were obtained. Bronchial P'close values were –24, –6, and –38 cm H2O, respectively (Table 5).


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  		TABLE 5. Results of fitting analysis for each infant with bronchomalacia on a linear regression model and percentage reduction of the cross-sectional area of the main bronchus

 
Results of Static Pressure/Area Assessment in Infants without Tracheomalacia
Results of the fitting analyses of pressure/area relationships of the trachea for the infants without tracheomalacia are presented in Table 6. Because no reduction of the tracheal cross-sectional area was observed during the apneic test in an infant without tracheomalacia (N4), P'close was unable to be obtained. In the other three control infants, P'close ranged from –34 to –136 cm H2O. Relatively lower R2 values indicate inaccuracy of the linear regression model. A cross-sectional area of the trachea was reduced by less than 40% in all infants.


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  		TABLE 6. Results of fitting analysis for each infant without tracheomalacia on a linear regression model and percentage reduction of the cross-sectional area of the trachea

 
Reproducibility of the P'close Measurements
Apneic testing was repeated in four infants with tracheomalacia to confirm reproducibility of P'close measurements (Figure 4). A second apneic testing was performed after the lungs were manually ventilated for 1 to 2 minutes. P'close differences between the first and second tests were less than 2 cm H2O in all cases (Table 4).



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  		Figure 4. Reproducibility of static pressure/area measurements. P'close differences between the first and second tests were less than 2 cm H2O in all cases.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Static pressure/area relationships of the trachea were successfully obtained from infants who were anesthetized and paralyzed with and without tracheomalacia. Cross-sectional areas of the trachea were observed to vary with changing airway pressures, in the range of 10 to –10 cm H2O. In infants with tracheomalacia, a linear regression model well represented the dependency of cross-sectional areas on airway pressure and provided estimated closing pressures (P'close) of the trachea (ranging from –8 to –27 cm H2O). This accounted for the clinical observation that infants with tracheomalacia rarely presented impaired respiratory events during spontaneous breathing, but rather developed a severe cyanotic spell during crying and coughing. Changes in the tracheal cross-sectional area during the step reduction of the airway pressure were less than 40% in infants without tracheomalacia, and the P'close estimation from the linear regression appeared to be inaccurate in infants with a less collapsible trachea.

Method Advantages
Invention of an ultrathin endoscope allows advanced diagnosis of tracheal narrowing in small infants with tracheomalacia (3, 4). Potential and inherent problems of this diagnostic endoscopic evaluation, however, are difficulty in cross-sectional area measurements during dynamic tracheal narrowing and lack of intrathoracic pressure control.

Various parameters presenting collapsibility of the trachea have been reported by measuring tracheal cross-sectional area with sophisticated imaging techniques at various intra-thoracic pressures. Suto and Tanabe (5) assessed tracheal collapsibility in the adult patients with tracheomalacia by measuring maximum and minimum cross-sectional areas of the trachea during coughing as well as forced expiration and inspiration using dynamic magnetic resonance imaging. Rozycki and colleagues (6) assessed collapsibility of the trachea by obtaining the smallest/largest airway ratio during respiratory cycle.

Reproducibility and accuracy of these methods, however, significantly depend on intrathoracic pressure developed during the measurements. Infants with tracheomalacia requiring mechanical ventilation are often administered sedatives, which may significantly depress coughing or crying as well as respiratory effort. Diffuse atrophy of the diaphragm has been reported in neonates with prolonged mechanical ventilation (7). Tracheal collapsibility may be underestimated in these conditions because of diminished intrathoracic pressure changes during the measurements. In contrast, in our study, the pressure/area relationship of the trachea was obtained under complete control of intratracheal pressure of infants who were anesthetized and paralyzed. By introducing the "tube law" concept, we succeeded in improving the quantitative assessment of tracheal collapsibility in infants with tracheomalacia as Panitch and colleagues successfully characterized collapsibility of excised newborn lamb trachea (2). Accordingly, the static pressure/area relationship of the trachea appeared to be useful for differentiation between infants with and without tracheomalacia. Furthermore, the P'close value obtained from the static pressure/area relationship well characterized collapsibility of the trachea. However, it should be recognized that the P'close estimation may not be accurate because of lack of validity regarding linearity of the pressure/area relationship below –10 cm H2O regardless of high R2 values in the Paw range examined in this study. In fact, a nonlinear pressure/area relationship was reported in neonatal lamb trachea (2). We believe that the P'close is a rough estimate at best in a clinical setting.

Methodologic Limitations
Several limitations exist in our assessment of tracheal collapsibility. First, control of the tracheal smooth muscle tone, which influences tracheal collapsibility, was insufficient (8). Midazolam, pancuronium, and sevoflurane have been reported to decrease tracheal smooth muscle tone (9, 10). Accordingly, collapsibility of the trachea may have been overestimated.

Second, during fixation of the endoscope position, the collapsible site may have shifted to the endoscope tip with airway pressure decrease. This may have led to overestimation of the lower airway pressure area, thereby resulting in underestimation of tracheal collapsibility.

Third, because our method only assesses collapsibility of the trachea and does not measure absolute cross-sectional area, it would be difficult to estimate the relative contribution of tracheal stenosis to the breathing abnormality, particularly in infants with combined tracheomalacia and tracheal stenosis.

Finally, deformation of the endoscopic image is inevitable for obtaining a wide-angle view, especially for a thin endoscope. The distance between the tip of the endoscope and the narrowing site varied between the infants, and we did not correct the endoscopic images for radial or "barrel-type" distortion, whereas the previous studies succeeded to minimize the image deformation with using sophisticated imaging techniques (2, 11). Accordingly, changes in cross-sectional area of the trachea were possibly underestimated with the airway narrowing and, therefore, underestimating tracheal collapsibility. Although we attempted to obtain tracheal images on the center of the view field as shown by the Figure 2, hopefully reducing the deformation problem, this strategy would have resulted in reduction of image resolution, possibly overestimating collapsibility of the trachea as we previously reported (12). Furthermore, we only measured the cross-sectional area once for each image. We believe that inaccuracy of manual cross-sectional tracing could be minimized by using the regression analysis, although the regression analysis does not minimize the systematic error produced by the image deformation.

Clinical Implications
The trachea of infants with tracheomalacia collapses when transmural tracheal pressure decreases with increasing intrathoracic pressure, particularly during forceful expiratory efforts. Reported maximal expiratory airway pressure during a crying effort is 125 ± 35 cm H2O in healthy infants on the average (0.06–3.76 years) (13) and 58 ± 17 and 44 ± 19 cm H2O in term and preterm neonates (14). Accordingly, the P'close range of between –8 and –27 cm H2O indicates that the trachea of infants with tracheomalacia easily collapses during crying or coughing, although it does not collapse during spontaneous respiratory cycle. In fact, all infants in our study presented apparent cyanosis only during crying and rarely presented respiratory events during spontaneous breathing.

Considering increases in maximal expiratory airway pressure with maturation, the dependency of the P'close on body weight suggests the presence of a threshold P'close value for each step of maturation. Although this possibly needs to be tested in a large sample covering full age range during maturation, it concurs with the fact that infants with tracheomalacia are often asymptomatic at birth and become symptomatic during development.

Interestingly, excised bronchi from cases of sudden infant death syndrome were reported to close at –11 cm H2O of intraluminal pressure (15), which is similar to the P'close obtained in the infants with tracheomalacia in this study. Although the etiology of sudden infant death syndrome is yet to be clarified and may include a variety of causes, increased collapsibility of the trachea could be one possible candidate for the pathogenesis of sudden infant death syndrome.

We believe that the unique method developed at our institute may be applicable to the evaluation of tracheal collapsibility improvement during maturation or after surgery, in addition to accurate diagnosis of tracheomalacia.

Although the main purpose of this study is to test validity of the pressure/area measurements for characterization of tracheal collapsibility in infants with tracheomalacia, a comparison of the tracheal collapsibility between infants with and without tracheomalacia is of great significance for increasing our understanding of pathogenesis of infantile tracheomalacia. Although results of this study suggest a possible difference of the static pressure/area relationships between infants with and without tracheomalacia, the number of normal infants is small, and their age and body weight are not matched to those of infants with tracheomalacia. Future studies should be directed to compare the static pressure/area relationships of the trachea of tracheomalacia infants with normal control subjects matched for age and body weight.

Three of eight infants had bronchomalacia in addition to tracheomalacia. Interestingly, compared with the tracheal collapsibility, similar (T4, T8) or even greater (T7) collapsibility of the main bronchus was found in these infants. Although no study has systematically evaluated contribution of bronchomalacia to morbidity in infants with tracheobronchomalacia, the increased collapsibility of the main bronchus might be partly responsible for the clinical symptoms because pure bronchomalacia was often identified in children with pulmonary atelectasis or wheezing (16, 17). Distribution of the collapsible region along the airway and contribution of each collapsible region to the pathological conditions are to be conducted in the future studies.

We conclude that tracheal collapsibility of infants with tracheomalacia can be quantitatively assessed by static pressure/area relationship of the trachea obtained under general anesthesia and paralysis.


   Acknowledgments
 
The authors appreciate the assistance of Sara Shimizu, M.D., who greatly helped to improve this article.


   FOOTNOTES
 
Conflict of Interest Statement: J.O. does not have a financial relationship with a commercial entity that has an interest in the subject of this article; S.I. does not have a financial relationship with a commercial entity that has an interest in the subject of this article; H.H. does not have a financial relationship with a commercial entity that has an interest in the subject of this article; M.S. does not have a financial relationship with a commercial entity that has an interest in the subject of this article; Y.N. does not have a financial relationship with a commercial entity that has an interest in the subject of this article; T.N. does not have a financial relationship with a commercial entity that has an interest in the subject of this article.

Received in original form December 11, 2003; accepted in final form July 3, 2004


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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