Tracheomalacia and Tracheobronchomalacia Challenging the diagnostic gold standard and refining the...

Tracheomalacia and Tracheobronchomalacia

Challenging the diagnostic gold standard and refining the definition

Melissa WeiMS4/MPH student

Diagnostic RadiologyJuly 2, 2009

Caveats:

• I am not a radiologist, and I do not regularly peruse radiology literature.

• I have taken a few epidemiology courses.

• As an epidemiologist in training, I enjoy counting, critiquing study methodology, and attempting at recommendations to hopefully advance research and ultimately patient care.

The focus of this presentation is on diagnosing and defining TBM:

• What are the diagnostic possibilities?• What are the advantages and limitations of

newer modalities (e.g. CT) over the gold standard, bronchoscopy, in diagnosing TBM?

• How well do these modalities correlate with bronchoscopy and with each other in diagnosing TBM?

• If the gold standard is replaced, how should the definition of TBM be revised so that it has a positive predictive value for symptomatic individuals and negative predictive value for healthy, asymptomatic individuals?

Presentation outlinePart I: BackgroundDefinition, Epidemiology, Classification, Pathophysiology, Clinical presentation

Part II: Diagnostic optionsHistorical perspective, bronchscopy as the current gold standard, CT, alternatives to CT, spirometry

Part III: Redefining TBMChallenges, suggestions

Part IV: Treatment (briefly)

Part I: What is Tracheomalacia?Malacia: softening of the tissuesTracheomalacia (TM): weakness of tracheal wall and/or

supporting tracheal cartilage, resulting in excessive expiratory collapse

Tracheobronchomalacia (TBM): mainstem bronchi also involved

Severity defined by extent of lumenal obstruction during expiration

– Mild: 50% lumen obstructed– Moderate: 75% lumen obstructed– Severe: posterior wall reaches anterior wall

Clinical significance: • Flaccidity of tracheal cartilage increases risk of airway

collapse especially with increased airflow demand

Lee 2009

Mild tracheomalacia45 year old asymptomatic man with normal pulmonary function

51% decreased cross-sectional area of tracheal lumen during expiration on axial dynamic CT

Normal oval-shaped tracheal lumen

Lee 2009

Severe tracheomalacia

Young child with compressed trachea from mediastinal vascular anomaly

Near collapse of tracheaMild tracheal compression from right-sided aortic arch (R)

EpidemiologyTBM in general adult population• Prevalence highest in men > 40 years (Jokinen 1977)

• Incidence increases with age (Jokinen 1977)

• 73% of TBM patients are between 50-80 years of age (Ikeda 1992)

TBM in symptomatic adults• 10-15% of patients referred to pulmonologist for

evaluation of chronic cough (Palombini 1999)

• 4.5% of 2150 patients who underwent bronchoscopy (Jokinen 1977)

– 1% with respiratory symptoms and bronchoscopy (Herzog 1958)

– 23% with history of chronic bronchitis and bronchoscopy (Jokinen 1976)

Classification Primary (congenital) TM <<

• Genetic eg polychondritis • Idiopathic “giant trachea” or

“Mounier-Kuhn” syndrome

Secondary (acquired) TM• Post-traumatic

• Intubation• Tracheostomy• External chest trauma• s/p lung transplantation

• Chronic inflammation/irritants• Emphysema• Chronic infection/bronchitis

• Chronic external compression of the trachea

• Tumors (benign or malignant)• Cysts• Abscesses• Aortic aneurysm• Vascular rings, undiagnosed in childhood

In kids, TM = #1 congenital tracheal anomaly; associated with transesophageal fistula

PathophysiologyNormal intrathoracic trachea

– Trachea dilates with inspiration, narrows with expiration– Reflects difference between intrthoracic and intraluminal pressures

Tracheomalacia = exaggerated physiologic process Accentuated changes in tracheal diameter

Intrathoracic problem (most common): excessive narrowing when Intrathoracic pressure > Intraluminal pressureEx) Forced expiration, Cough, Valsalva maneuver

Extrathoracic problem: negative intrapleural pressures transmitted to extrathoracic trachea due to pleural reflections upper airway collapses during inspiration

Atrophy of longitudinal elastic fibers of pars membranacea or impaired cartilage integrity airway soft, susceptible to collapse

Most common causes#1 Weakening of tracheal wall

– Intubation: recurrent, prolonged pressure necrosis, impaired blood flow, recurrent infections, mucosal inflammation

– High-dose steroids

#1 Inflammation/irritation of tracheal wall– Smoking– Recurrent infections: chronic bronchitis, pneumonia

3. Compression of trachea– Malignancy, abscess, cysts, goiter

4. Direct damage to tracheal wall– External trauma or surgery

5. Vascular malformations– Double aortic arch, R aortic arch with aberrant L subclavian a,

ligamentum arteriosum

1. Symptoms are nonspecific (Jokinen 1977, Carden 2005)

• Dyspnea (63-75%)• Chronic cough (50%)

- sputum production- “seal like” or barking cough

• Hemoptysis (33%)• Episodic choking; syncope with forced exhalation and cough

2. Concurrent respiratory disease common (Carden 2005)

• Chronic bronchitis• Emphysema• Bronchial cancer• Recurrent respiratory infection• Asthma

3. Pts may be Asymptomatic …… until stressed by infection (bronchitis, pneumonia)- Intubated patients: masked by PPV maintaining airway

Clinical presentation

4. Physical exam findings• Respiratory distress• Inspiratory wheezing• Stridor• Barking cough• Deep breathing, cough, and Valsalva manuever

elicit airway collapse

Clinical presentation

• Laryngomalacia• Subglottic stenosis• Vocal cord paralysis

TBM is commonly misdiagnosed as:• COPD • Asthma • Among 80 patients with suspected or diagnosed TBM, 40% had COPD and

24% had asthma (Loring 2007)

“Although TBM and COPD coexist, the implications of this coexistence are not fully understood.” -Kandaswamy 2009

Differential diagnosis

Imaging modalities• Plain radiographs – not diagnostic• Historical modalities• Flexible bronchoscopy – current gold standard• Standard spiral CT• Dynamic expiratory multi-detector CT (MDCT)• MRI• Virtual bronchoscopy

Pulmonary function tests• Research ongoing, not diagnostic

Part II: What are the diagnostic options?

Limited use of plain radiographs to diagnose TBM• TBM is a dynamic process accentuated by

forced expiration• Cannot visualize on anterioposterior or lateral

chest radiographs

Exception• TBM secondary to compression from other

structures (e.g. mediastinal goiter, tumor) may be visualized

Imaging: Plain radiographs

• Cinetracheograms to visualize tracheal flutter

• Fluroscopy to estimate tracheal diameter• Tracheograms and bronchograms

Replaced by bronchoscopy, which is more sensitive for diagnosing TBM

Historic modalities: We’ve come a long way

• Visualize dynamic tracheal or bronchial collapse• Trachea may also be widened• Flexible bronchoscope over rigid

- Patient can breathe spontaneously and perform additional maneuvers to elicit collapse of the airways

• Expiratory effort to achieve airway wall collapse through maneuvers (deep breathing, forced expiration, straining, coughing, others) has not been standardized

Bronchoscopy is the current gold standard for diagnosing TBM

Bronchoscopy

Carden 2005

• Invasive, requires general anesthesia (rigid bronchoscopy) or local anesthesia (flexible bronchoscopy), and more than half of patients sedated

• Contraindications: ongoing arrhythmias or refractory hypoxemia

• Complications: • 1.3% of 4,000 flexible bronchoscopies (Pue 1995)

• 25% of complications due to premedications or anesthetic drugs (Credle 1974)

• Bleeding, infection

However, bronchoscopy has limitations

• Noninvasive• Fast, entire central airway imaged in a few

seconds• High spatial resolution, great anatomic

coverage• Opportunity for multiplanar reformation and

2D, 3D reconstruction images• Can observe additional imaging features

characteristic of TBM

CT can also be used to diagnose TBM and has several advantages

over bronchoscopy

Carden 2005

2D CT reconstruction Inhalation Exhalation

Segmental tracheal collapse

An important advantage of CT over bronchoscopy:

Additional radiographic abnormalities can be identified to

characterize TBM.

A few observations include …

Dynamic expiratory CT64 year old man with chronic cough

“Frown sign” in 50% TBM patients

Trachea is collapsed with crescentaric, frown-like configuration of the airway lumen

Lee 2009

“Lunate configuration”

Lee 2009

Coronal diameter is widened compared with sagittal diameter

Dynamic expiratory CT 71 year old woman with dyspnea, chronic cough

Air trapping has also been observed in TBM patients

Gilkeson 2001

Focal collapse of proximal right upper lobe bronchus. Right upper lobe is hyperlucent, consistent with air-trapping

52 year old man with idiopathic TM and persistent cough after mainstem bronchi stent

What is the extent and distribution of air trapping in TBM?

First study to report air trapping in TBM:“Air trapping was observed with a higher frequency and greater severity in patients with TBM than in the control group.” -Zhang 2004

• Retrospective case-control study• 10 bronchospically diagnosed cases TBM (5 men,

5 women, aged 42-79 y, 1 asthma, 3 emphysema)• 10 controls (3 men, 7 women, aged 27-75 y, 5

asthma, 1 emphysema)

• Statistical analysis: Mann-Whitney Wilcoxon U testof the median group value for cases vs. controls

Cases: 10/10 air trappingmedian score 5 (range 2-12)

Controls: 6/10 air trapping, median score 2 (range 0-3)

“MEDIAN TOTAL air trapping score” was significantly higher in TBM group vs. control group (p<0.001)

Zhang 2004

Is air trapping specific to TBM cases?• There was also air trapping in the control group

(regardless of history of chronic airway disease), although less severe (median score 5 vs. 2)

Distribution:• Air-trapping in cases was mostly lobular (8/10) but

not always (2/10)• Lobular air trapping was also observed in 3/10

controlsLimitations of Zhang 2004: • Small sample size• Wilcoxon is a parametric test of the median

difference between the groups. It is highly influenced by outliers.

*

To check the appropriate use of the Wilcoxon test of the median difference between cases and controls:

After assessing for outliers (case scores 11 and 12), there was no change in the median score, although the mean decreased from 6 to 4.6. Thus, I agree with Zheng et al. that there is a statistically significant difference between the median air-trapping score in cases vs. controls after a sensitivity analysis for potential outliers.

0 1 2 3 4 5 6 7 8 9 10 11 12

0 1 2 3 4 5 6 7 8 9 10 11 12

Cases: median score 5, mean 6, range 2-12

Controls: median score 2, mean 1.6, range 0-3

* ** ** * * * *

****** ****

Air trapping score (Max 12)

Given the advantages of CT…

What is the quality of CT studies, and how well do CT findings

correlate with the gold standard, bronchoscopic diagnosis of TBM?

Single-detector spiral CT scan: compare cross-sectional area of the trachea during inspiratory and end-expiratory CT scan– Aquino (2001), case-control study

Multi-detector helical CT scan: captures continuous expiratory phase of respiration– Gilkeson (2001), case series

CT vs. bronchoscopy landmark studies

Aquino (2001), case-control study• N=12 bronchoscopically diagnosed cases acquired TM;

after excluding patients whose TM not seen on CT, N=10 (6 men, 4 women, aged 42-84 y), 23 healthy controls (15 men, 8 women, aged 27-57 y)

• Statistical analysis: t-test, receiver operator curve• Cross-sectional area between inspiratory and expiratory

CT more sensitive and specific than sagittal and coronal diameters for detecting TM

• >18% reduction in upper trachea and >28% reduction in midtrachea cross-sectional area had positive predictive value 89-100%, negative predictive value 95-100%

Suggests end-expiratory imaging may require lower threshold criterion than ≥ 50% narrowing especially if sagittal or coronal diameters used

Expiratory CT vs. bronchoscopy

Aquino 2001

Percent change in tracheal area not always >50% among Aquino study of bronchospically confirmed TBM cases

Aquino 2001

Percent change in upper and mid trachea cross-sectional area greater in cases than controls but not always > 50%

Coronal (Table 4) and saggital diameters (Table 3 not shown) lower than cross-sectional area (Table 2) and < 50%

Strengths:• Bronchospically confirmed TM cases• Automated measurement of tracheal lumen and

cross sectional area

Limitations:• Selection bias: Appropriate exclusion of 2

bronchospically confirmed TM cases (2/12)? Inclusion would decrease reported positive and negative predictive values

• Small sample size … but use of student’s t-test assumes normality

• Potential investigator bias: radiologists not blinded• Similarity between cases and (younger) controls?

Aquino strengths & limitations

Gilkeson (2001), case series• 13 patients with “suspected” TBM (7 men, 6 women,

aged 14-88 y, 3 asthma)• Multidetector inspiratory—dynamic expiratory CT and

spirometry performed on all patients• Fiberoptic bronchoscopy performed on 6/13 patients • Statistical analysis: Not provided!• Results: All patients had airway collapse on inspiratory

—dynamic expiratory CT that was highly correlated with degree of collapse on bronchoscopy

• Conclusion: supports more conservative diagnostic threshold of >50-70% narrowing on forced expiration to diagnose TBM

Dynamic MDCT vs. bronchoscopy

Gilkeson 2001

Note:

Bronchos-copy results for 6/13 patients

Exact value of collapse not given for CT and bronchos-copy, only ranges e.g. 50-75, 75-100

• Selection bias: “Our cohort was a highly selected patient population without healthy control subjects”

• Potential outcome misclassification for 7/13 patients without bronchoscopy: patients with “suspected TBM”

• Investigator bias: patient histories known, non-blinded • Small sample size: N=6 with both bronchoscopy & CT• Case series, no control group, cannot evaluate

statistical significance of results• Nebulous statistical methodology

– CT and bronchoscopy values given as 25 percentage point ranges (e.g. 50-75, 75-100), not exact values

– Correlation coefficients not provided

Questionable internal & external validity generalization

Limitations of Gilkeson’s dynamic MDCT vs. bronchoscopy case series study

To illustrate how selection bias could impact results in a case series study:

TBM Case Control

+ TBM

- TBM

Dynamic

MDCT

a b

c d

Increased patients in box “a” (patients with TBM on bronchoscopy and dynamic CT, most likely in this study) or fewer patients in box “c” would result in an increased odds that patients have TBM by bronchoscopy (outcome) given TBM by MDCT (exposure)

Bronchoscopy

Odds ratio, OR = a * d = a * d = OR b * c b * c

There are also different types of CT studies. How well do they correlate with

each other for diagnosing TBM?

Dynamic vs. end-expiratory CT:

–Baroni (2005)

–Ferretti (2008)

Baroni (2005), case series• N = 34 with CT diagnosis of TBM; after exclusions

N = 14 (11 men, 3 women, aged 19-79 years)• Airway collapse measured by multi-detector row CT

at end inspiration, dynamic expiration, and end expiration at aortic arch, carina, bronchus

• Statistical analysis: paired two-tailed t test • Dynamic expiratory CT elicited significantly greater

airway collapse than standard end-expiratory CT for all individuals at all three levels (all p < 0.005)– Biologically consistent with fact that dynamic

expiration produces higher level of intrathoracic-extratracheal pressure than end expiration

Dynamic CT vs. end-expiratory CT

Bronschospic results available for N =10

Baroni 2005

From bronchoscopy:• 7/14 with TBM• 3/14 without TBM• 4/14 data unavailable

Baroni 2005

TBM

TBMTBM

TBMNo TBM

No TBM

Bronch

>

TBM No TBM

Bronchoscopy 3 2

Dynamic Expiration 2 1

End Expiration 1 2

Baroni 2005

TBM

TBM

TBM

TBM

TBM

No TBM

No TBM

Bronch

>

TBM No TBM

Bronchoscopy 5 2


End Expiration 1 2

Baroni 2005

TBMTBMTBM

No TBM

No TBM

Bronch

>

TBM No TBM

Bronchoscopy 4 2


End Expiration 0 1

TBM

Baroni cont. Dynamic vs. end expiratory imaging:

• Airway collapse was consistently greater in dynamic expiration compared with end expiration – Dynamic: More often diagnosed TBM correctly

… but also over-diagnosed TBM in non-cases– End expiration: More likely to miss TBM

… but never diagnosed TBM in non-cases• When using the criteria of >50% reduced cross-

sectional area, there was disagreement in TBM diagnoses in 5/9 (56%) patients at the aortic arch, 6/10 (60%) patients at the carina, 6/7 (86%) patients at the bronchus intermedius

• Limitations: selection bias, small sample size with 20/34 excluded, non-blinded, lumens hand-traced

Ferretti (2008), prospective study• 70 patients with suspected TBM• Central airway collapse measured from the

percentage change in area and diameter between end inspiration, and two expiratory techniques at:– Trachea at three levels– Right and left main bronchi, sagittal diameter

• Airway collapse significantly greater with dynamic expiratory imaging than end-expiratory imaging: – Lower trachea (26% vs. 17%, p<0.009)– Right main bronchus (25% vs. 14%, p<0.01) – Left main bronchus (25% vs. 13%, p<0.01)

Dynamic expiratory consistently diagnoses more patients with TBM than end-expiratory imaging

Dynamic CT vs. end-expiratory CT

Limitation 1:• Healthy, asymptomatic individuals may demonstrate

expiratory collapse that exceeds the criterion for TBM

Recommendations• Use a more conservative threshold of 70% in

dynamic CT as indicative of TBM• Correlate MDCT results with respiratory symptoms

and functional impairment• Further research that stratifies by age, sex,

race/ethnicity, coexistent pulmonary disease, and other risk factors for TBM

What are the limitations in using CT imaging to diagnose TBM?

Lee 2009

Limitation 2:• Potential “double dose” radiation exposure in paired

inspiratory-expiratory CT

Recommendations• Low-dose technique possible without compromising

image quality – High contrast between air-filled trachea and soft

tissue structures already present– No difference observed between standard (240-

260 mA) and low-dose (40-80mA) radiation for assessing tracheal lumen during dynamic expiration (Zhang 2003)

CT limitations

Lee 2009

1. Improved ability to diagnose TBM with CT? Sparse studies afflicted by selection bias and investigator bias report correlation between CT and bronchosocpy, but more data warranted

2. Should MDCT be the new gold standard? Consider both strengths and limitations of CT

3. How/When is there consensus to replace the gold standard? Historically not always data-driven, may be influenced by subspecialty groups

4. If CT replaces bronchoscopy, how should the definition and diagnostic criteria of TBM be revised?

Should MDCT replace bronchoscopy?

Beyond CT, what alternative diagnostic imaging modalities

have been studied?

• Dynamic MRI during forced expiration and cough• Preferred method for evaluating extrinsic airway

abnormalities (e.g. vascular compression syndromes) in children (Faust 2002)

• Advantages: Repeated assessment during multiple respiratory maneuvers without ionizing radiation exposure

• Disadvantages: COST!!

Sensitivity and specificity compared with bronchoscopy and CT? To be demonstrated in case-control studies

Imaging: MRI

Carden 2005

MRI child with vascular compression syndrome

Narrowed trachea secondary to vascular entrapment

Suto1998

Among adults, MRI during coughing showed significantly greater collapsibility in bronchospically confirmed TBM cases (N=6) compared with healthy controls (N=13) (p<0.05)

Axial MRI during coughing also resulted in significantly greater collapsibility than forced expiration and inspiration for both cases and controls (p<0.01)

44 year old man with bronchospically confirmed TM

Suto1998

forced inspiration forced expiration coughing

Virtual bronchoscopy57 year old woman with suspected congenital lobar emphysema of right lung

Gilkeson 2001

Mild narrowing but patent right middle (M) and lower (L) lobe bronchi

Complete collapse of lower lobe orifice (authors state this was not appreciated on axial CT imaging)

• CXR - assess baseline chronic disease or new infection• However, cannot diagnose TBM

• Bronchoscopy, flexible - historical gold standard• Dynamic CT - new standard???

• Diagnositic threshold should be higher in dynamic CT but lower for end-expiratory CT

• MRI• Multiple maneuvers and assessments possible without

radiation exposure• Significantly greater cost

• Virtual bronchoscopy – more studies warranted

Imaging summary

• Yes, but many findings are non-specific to TBM- Decreased FEV1

also seen in obstruction- Low peak flow rate with a rapid decrease in flow

also seen in obstruction- Flow oscillations

also seen in obstructive sleep apnea, structural or functional larynx abnormalities, neuromuscular disease

- Elevated airway resistance- Inspiratory limb shape preserved

Do TBM patients exhibit abnormalities in pulmonary function tests?

Unique “notch” in forced expiratory spirograms in TBM• “Break” or “notch” in expiratory phase of flow-volume

curve thought to represent the point of major airway collapse after dead space air volume is emptied

• First described by Koblet and Wyss (1955) and observed in 3 subsequent studies

• Limitation: Moderate to severe emphysema patients display similar notch, regardless of concurrent TBM

Unreliable for diagnosing TBM

Are there TBM-specific findings in pulmonary function tests?

Carden 2005

Flow-volume loops in TBMThere is a rapid decline in maximal expiratory flow following a sharp peak associated with collapsed central airways from negative transmural pressure.

Normal inspiratory profile from dilation of central airways during treatment with positive transmural pressure.

Most recent studies report NO association• Obstruction from spirometry is proportional to severity

of TBM (Nuutinen 1977)• No correlation between obstruction and TBM severity

(Gilkeson 2001)• No correlation between central airway collapse (80 suspected

and confirmed TBM cases) and degree of obstruction via FEV1. Central airway collapse was observed regardless of expiratory flow limitation during quiet breathing. One cannot assume central airway narrowing (especially during quiet exhalation) in patients with obstructive airway disease. Likewise, symptomatic central airway narrowing may exist in patients without significant airflow obstruction (Loring 2007)

Is there an association between obstruction findings in spirometry and

severity of TBM?

Part III:How should the definition and diagnostic

criteria for TBM be revised to improve sensitivity and specificity

of symptomatic patients who may benefit from treatment?

• Lack of clarity in definitions, measurement criteria and terminology

• Need to establish normal vs. abnormal narrowing of central airways

• TBM is a spectrum• Patients with TBM present with a range of symptoms• Coexistence of asthma, COPD among TBM patients• Currently no universally agreed upon classification system

Proposed system by Murgu 2007 ….

Challenges in diagnosing TBM

FEMOS classification

• Functional status

• Extent of abnormality

• Morphology

• Origin

• Severity of airway disease

Murgu 2007

FEMOS classification system

Functional status – modified World Health Organization functional classification

• Class I (F1) – no limitation

• Class II (F2) – mild limitation of physical activity

• Class III (F3) – marked limitation of physical activity

• Class IV (F4) – unable to perform any physical activity at rest

Murgu 2007


Extent of abnormality based on location and distribution of the abnormal airway segment viewed on bronchoscopy

• Normal (E1) – no airway abnormality• Focal (E2) – abnormality present in one main or

lobar bronchus or one tracheal region (upper, mid or lower)

• Multifocal (E3) – abnormality present in two contiguous or at least two non-contiguous regions

• Diffuse (E4) – abnormality present in more than two contiguous regions

Murgu 2007


Origin is the etiology of the airway abnormality

• Idiopathic – no underlying etiology identified

• Secondary – result of an illness or other pathological process

Murgu 2007


Severity of airway collapse based on the degree of airway lumen reduction during expiration as observed in bronchoscopy

• Normal (S1) – no abnormal airway collapse

• Mild (S2) – 50-75% expiratory airway collapse

• Moderate (S3) – 75-100% expiratory airway collapse

• Severe (S4) – 100% expiratory airway collapse and airway walls make contact

Murgu 2007

Suggestions for future TBM studies

• Prospective cohort studies ideal to decrease selection bias, but challenging to conduct

• To decrease bias in case control studies: – Careful selection of control group (ideally identical

to cases by all characteristics except TBM)– Large sample size, test normality assumption– To reduce investigator bias, blinding to subjects’

case status and history– Automated measurement of tracheal lumen and

cross-sectional area with exact values provided– Review by at least two radiologists and report

kappa statistic of inter-observer agreement

Part IV: Treatment (Briefly)Asymptomatic No treatmentSymptomatic:

– Supportive care – Control bronchospasm– Treat primary problem eg obstructive disease

Critical condition:– Positive-pressure ventilation– CPAP increases FVC and reduces airway collapse (Ferguson 1993)– Facilitate mobilization of secretions

Severe cases may benefit from surgery:– Tracheostomy: bypass malacic segment or tube. May be complicated by

recurrent tracheobronchitis, stenosis at stoma site – Ceramic rings: Longest successful follow-up in 16/16 patients after 6.4

years (Amedee 1992)– Stents (silicone > metal): patients reported immediate improvement in

symptoms but PFTs declined at mean 15 months follow-up after stenting (Gotway 2002). Center and operator dependent. High complications. More research needed.

After tracheoplasty

Carden 2005

Lessons from Dr. Gosselin

Resist algorithms

&binary thinking

People are like

snowflakes

Carden 2005

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with expiratory central airway collapse. Respirology 2007;12:543-50. 18. Palombini BC, Villanova CA, Araujo E, et al. A pathologenic triad in chronic cough:

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